z zyxwvutsrqp zyxwvutsrq zyxw zyxwv zyxwvu Botanical Journal of the Linnean Society (200l), 137: 1-29. With 71 figures doi:l0.1006/boj1.2001.0443, available online a t httpj'/www.idealibrary.com on I D E 0 zy A morphological and anatomical survey of Virectaria (African Rubiaceae), with a discussion of its taxonomic position S. DESSEIN'*, S. JANSEN', S. HUYSh"S1, @ E. ROBBRECHT2 and E. SMETS' Received April 2000; accepted for publication January 2001 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 'Laboratory of Plant Systematics, Institute of Botany and Micmbiology, K. U. Leuuen, Kasteelpark Arenbelg 31, B-3001 Leuuen, Belgium 2National Botanic Garden, Domein van Bouchout, B-1860 Meise, Belgium zyxwvuts A detailed morphological and anatomical study of the tropical African genus Virectaria is presented. The observations are used to characterize the genus, to propose a key to all eight species, and to unravel the relationships between the species using cladistics. A taxonomic survey of the genus is also given. Verdcourt's infraspecific taxa based on calyx morphology in X rnujor are adopted, but it was found that morphological distinction is correlated with ecological, habit and distributional differences. Hence, it is better t o recognize Verdcourt's varieties spathuluta and major as subspecies of X major. The problematic systematic position of the genus is discussed in detail. New evidence is given for the exclusion of the genus from the Hedyotideae and Ophiorrhizeae (subfamily Rubioideae). The recently proposed position in the Sabiceeae (subfamily Ixoroideae) is not convincing either, since none of the genera included in the Sabiceeae matches Virectaria with respect to pollen, fruit, flower and growth habit. Exclusion from the Rubioideae and a position near the Sabiceeae is supported by lack of raphides, seed anatomy, placentation, stipule morphology and molecular evidence. Molecular data from a larger number of taxa are needed to confirm the position of the genus. 0 2001 The Linnean Society of London ADDITIONAL KEY WORDS: cladistic analysis - fruit - ovary - pollen morphology - Sabiceeae - seed anatomy wood anatomy. cells with only slight thickenings. Indeed, several authors have discussed the taxonomic position and Verdcourt (1975) even erected a monogeneric tribe (Virectarieae) for this aberrant genus. The aims of the present study are (1) to present a thorough documentation of the genus' character states (including pollen morphology, wood anatomy, seed coat anatomy, gynoecial structure), (2) to provide a hypothesis for intraspecific relationships using cladistic algorithms, and (3) to discuss the systematic position of Virectaria on the basis of all data available. INTRODUCTION Virectaria Bremek., until 1952 known as Virecta Afzel. ex Sm., consists exclusively of tropical African species. It is a Guineo-Congolian genus, having its highest diversity in Lower Guinea, but it also occurs in the Zambezian Region. Verdcourt (1953) provided a revision in which he defined five species, but three more were added later (Halle, 1966; Hall, 1972). All species are herbaceous or semi-woodyand possess a fruit dehiscence type that is unique for the family; the splitting into one persistent and one deciduous valve allows recognizing the genus a t first glance. In habit, Virectaria strongly resembles African Hedyotideae such as Parapentas and Otomeria, but it lacks some diagnostic features of that tribe, viz. raphides, articulate hairs, heterostylous flowers and exotestal TAXONOMIC HISTORY Virecta was established by Smith in Reed Cyclopaedia (1817). The name Virecta is derived from 'virectum' (a green place), and refers to the agreeable greenness of the leaves. New species were described by de Candolle (1830), Don (1834), Hiern (1877), Baillon (1880), and Schumann (1896). Bremekamp (1952) renamed Virecta zyxwvutsrq * Corresponding author. E-mail: steven.dessein@bio.kuleuven.ac.be 0024-4074/01/090001+ 29 $36.00/0 1 0 2001 The Linnean Society of London 2 zyxwvutsrqp zyxwvutsrq S. DESSEIN ET AL. Bremer & Thulin suggested affinities between Erectaria and Tamridaea, a genus first described in the same paper for an endemic species from Socotra formerly placed in Pseudomussaenda. The position of Erectaria near Sabicea was confirmed by molecular data of the rpsl6 intron @ova, 1999). In his analysis Sabicea and Erectaria form a clade with a very strong jackknife support. MATERIAL AND METHODS MATERIAL This study is based on the examination of herbarium specimens of BR, WAG, and K, and fixed material preserved in 50% alcohol. Before the pickled material was investigated it was transferred t o 70% alcohol. Dried material was first rehydrated with the wetting agent Agepon (1:200). Illustrations were prepared from the following collections (* =pickled material): Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Afzel. ex Sm. as Erectaria, because the type species of Erecta L.f. was transferred t o Sipanea Aubl.; he also questioned the taxonomic position of the genus. Verdcourt (1953) revised the genus and reduced the number of species from twelve to five. Later, Halle (1966) recognized two more species in Gabon, and Hall (1972) added a new species from Ghana. The genus ‘Erecta Afzel. ex Sm.’ was included in the tribe Hedyotideae in all classical systems of the Rubiaceae; both Hooker (1873) and Schumann (1891) placed it in between Pentas and Otomeria. Bremekamp (1952) excluded the genus from the Hedyotideae, mainly because it lacks raphides. He proposed a new tribe Ophiorrhizeae for the tropical Asiatic Ophiorrhiza and Spiradiclis, and the tropical African Virectaria. Verdcourt (1958) investigated the three genera and found raphides in Spiradiclis and Ophiorrhiza. He maintained the Ophiorrhizeae near the Hedyotideae but excluded Virectaria, suggesting (without formally establishing) a monogeneric tribe in a position remote from the Hedyotideae. In his revision of Erectaria (Verdcourt, 1953),he considered the genus t o be closely related to the Rondeletieae and with Sipanea and Limnosipanea, two genera which Verdcourt referred t o the Hedyotideae. In 1958 Verdcourt referred these two genera to the Rondeletieae. He stated that “the similarity between Erectaria and Sipanea may also be accidental since there are testa and aestivation differences” (Verdcourt, 1958: 243). He also rejected affinities between Erectaria and the tribe Pomazoteae, an affinity suggested by Bremekamp (1952). In 1975, Verdcourt erected the monogeneric tribe Virectarieae and placed it in the subfamily Cinchonoideae, i.e. away from the Hedyotideae, which he included in the subfamily Rubioideae. Bridson & Verdcourt (1988) placed the tribe Virectarieae near the tribe Rondeletieae. Halle (1966) treated Virectaria as a member of the Hedyotideae, but he stated that it takes a rather isolated position because of the lack of raphides and the particular features of the stigmata and the fruit dehiscence. Darwin (1976) suggested returning Ophiorrhiza to the Hedyotideae. Robbrecht (1988, 1994) accepted the Ophiorrhizeae and placed them next to the Hedyotideae. He stated: “I also support that Erectaria may be returned to the Hedyotideae, since its removal was based only on the absence of raphides [a feature which he argued to have no absolute taxonomic value]; otherwise, this herbaceous to semi-woody genus fits extremely well within the Hedyotideae”(Robbrecht, 1988: 161). Molecular evidence (rbcL sequences; Bremer & Thulin, 1998)recently referred Virectaria t o the Sabiceeae, a tribe that was resurrected by Andersson (1996), and redefined by Bremer & Thulin (1998). Moreover, zyxwvut Erectaria angustifolia (Hiern) Bremek.: Cameroon, Nemba & Thomas 321 (BR 807327), Figs 14,16,66; Cameroon,Letouzey 13809(BR 807324), Figs 51-53. Erectaria belingana Halle: Gabon, Bos, uan der Laan & Nzabi 10692 (BR 810176), Figs 3, 6-7. Erectaria herbacoursi Halle: Gabon, de Wilde, Arends, Louis, Bouman & Karper 560 (BR 808005), Figs 62, 68. Erectaria major (K. Schum.) Verdc. subsp. major: Congo, Lebrun 4242 (BR 807322), Figs 14, 15; Rwanda, Tmupin 10367 (BR 808010)*, Figs 1, 2, 33-40, 4 1 4 4 , 48; Rwanda, Troupin 9698 (BR 808013)*, Figs 3-5, 9-11. Erectaria major (K. Schum.) Verdc. subsp. spathulata (Verdc.) Dessein & Robbr.: Congo, Troupin 3397 (BR 901747)*, Figs 18-32; Congo, Louis 10971 (BR 807355), Fig. 12. Erectaria multiflora (Sm.)Bremek.: Congo, Staner 1415 (BR 809944), Figs 8, 45, 46. Erectaria pmcumbens (Sm.) Bremek.: Congo, Louis 3141 (BR 807342), Fig. 47. Erectaria sal icoides (C .H. Wright) Bremek.: Gabon, Bates 527 (K), general morphology. Erectaria tenella Hall: Ghana, Morton A2686 (K), seed morphology and anatomy, Figs 54, 59, 60. GEOGRAPHY The distribution maps are based on BR and a small number of WAG specimens (Appendix 1)and the specimens cited by Verdcourt (1953, 1993), Hutchinson (1963), Halle (1966), Hall (1972) and Bridson & Verdcourt (1988). The database containing the data of the BR specimens can be obtained from the corresponding zyx zy SURVEY OF WRECTARIA 3 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zy zyxwvu zyxwvuts Figures 1-8. Vegetative features (SEM) of Virectaria. Fig. 1. R major subsp. major: external indumentum, portion of four hairs. Fig. 2. R major subsp. major: broken hair of external indumentum showing the wall layers. Fig. 3. R belingana: leaf-blade below showing main vein. Fig. 4. R major subsp. major: leaf-blade below showing stomata. Fig. 5 . R major subsp. major: leaf-blade above showing papillate epidermis. Fig. 6. R belingana: cross-section of leaf-blade. Fig. 7. R belingana: node showing petioles and entire interpetiolar stipule. Fig. 8. R multiflora: node showing petioles and bifid interpetiolar stipule. Scale bar = 1mm. author. For each country, specimens are arranged according to degree squares. This degree reference system is adopted from De Block (1998). ‘Congo’ stands for the Democratic Republic of the Congo; Congo Brazzaville is indicated as ‘Congo (Braz)’. The chorological division of Africa follows White 4 S. DESSEIN ET AL. 9 • Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Figures 9-16. Leaf (Figs 9-11, LM) and wood anatomy (Figs 12-16, LM) of Virectaria. Fig. 9. V. major subsp. major. transverse section (TS) of leaf showing papillate upper epidermis, one layer of pallisade parenchyma, loosely arranged spongy parenchyma, and lower epidermis. Scale bar =200 ~Lm. Figs 10, 11. V major subsp. major: leaf lamina showing main vein shown in TS (detail in 11). Scale bar = 20 ~m. Fig. 12. V. angustifolia: TS wood. Scale bar = 200 J.llll. Fig. 13. V. major subsp. spathulata: TS wood. Scale bar = 200 J.lill. Fig. 14. V. major subsp. major: TS wood. Scale bar = 200 jliD. Fig. 15. V major subsp. major. tangential section of wood. Scale bar = 200 ~m. Fig. 16. V angustifolia: tangential section of wood. Scale bar = 200 Jilll. (1978 (Afromontane Region), 1979 (Guineo-Congolian Region), 1993). For convenience, however, the classical terms 'Region' and 'Domain' are preferred above White's intricate categories such as 'regional centre of endemism' and 'subcentre of endemism'. SEED MORPHOLOGY AND ANATOlVIY For morphological observations, the seeds were mounted without treatment on stubs and investigated with a SEM Jeol6400. To remove the outer tangential wall of the exotesta cells, the seeds were rehydrated in zyx zyxwvut SURVEY OF VIRECTARIA 5 based on the species descriptions by Verdcourt (1953), Halle (1966) and Hall (1972), and the information available on the herbarium specimens. Erectaria species are essentially herbaceous plants. A few taxa, however, show a trend to a more robust and woody growth form. Four species have adaptations to a rheophytic environment, while others, with a larger ecological amplitude, are less specialized. POLLEN MORPHOLOGY V angustifolia shows adaptations typical of rooted Acetolysis was performed following Reitsma’s (1969) rheophytes (cf. Van Steenis, 1981). The root system of ‘wetting agent’ method (10min a t 90OC). After acethis small annual or short-lived perennial consists of tolysis the sample from each specimen was partitioned small petrophiles with taproots that penetrate rock into two subsamples, one for the LM and one for the crevices. From the rather widened base, several erect SEM. Pollen for SEM was stored in ethanol 70%. The stems arise which bear many small lanceolate leaves. grains suspended in alcohol were mounted on a stub, V salicoides resembles this growth habit, but is larger air-dried and coated with gold, using a SPI-MODULETM and more robust. These two species are limited to sputter coater. Observations were made with a Jeol riverbeds. 6400 SEM. The glycerin jelly slides were observed with Two other species, X tenella and X pmcumbens, a LM Leitz Dialux 20. Pollen was broken using glass grow predominantly near rivers or on shady hill slopes. beads as described by Huysmans, Robbrecht & Smets V tenella, a slender, prostrate herb, has a root system (1993). similar to that of X angustifolia; the leaves, however, Polar axis (P) and equatorial diameter (E) were are broader. V pmcumbens also is a low creeping or measured in about ten mature pollen grains with LM somewhat straggling herb up to 30 cm tall, but has a (magnification 1000). Other measurements were made root with a mass of fine rootlets. At some nodes up to on SEM micrographs. Terminology follows Punt et al. four axillary branchlets occur. (1994). The growth form of the four remaining species is less specialized; they are often found on hill slopes. X multiflora is a n annual herb with a n unbranched root. WOOD ANATOMY The stems, often woody a t the base, are 10-150cm Secondary xylem was sufficiently developed in three tall. Like X major, this species has a large ecological species to permit a wood anatomical study. Woody stem amplitude. It has been collected in grasslands, inparts (V. major: Lebrun 4242, 5mm; Louis 10971, undated wet places, slopes of rocky hills as well as in 8 mm; X angustifolia: Nemba & Thomas 321, 5 mm) V major resembles V multiflora but ruderal terrains. were taken from herbarium material. Wood blocks is perennial, forming a n erect or somewhat scandent were sectioned and macerated according t o standard herb or subshrub, 0.5-3 m tall and woody a t the base; methods (Jansen et al., 1998). Vessel element length subspecies decumbens has a more decumbent habit and fibre length were measured from macerations in and is only c. 75cm tall. Some collectors (e.g. Louis) 30 elements per sample. Terminology follows the IAWA reported a ‘lianescent’ growth for X major subsp. spalist (IAWA Committee, 1989). thulata, indicating the more slender growth form of this subspecies (cf. below). X belingana is an erect CLADISTIC PROCEDURES herb or subshrub up to 1.50m tall with highly branched Cladistic analyses were based on maximum parsimony pubescent stems. The ramifications of the branches (Farris, 1983) using PAUP 4.0 (Swofford, 1999). All are divaricate. X herbacoursi is a small herb with a analyses were run with equal weighted characters more or less straggling stem from which several erect (Appendix 2). The low number of terminals permitted stems arise up to 60cm tall. us t o adopt an exhaustive search algorithm. All multistate characters were treated as unordered. Bremer INDUMENTUM supports (Bremer, 1994) and bootstrap values were The external indumentum consists of eglandular, cylcalculated using PAUP 4.0. The data matrix is preindrical hairs (typology according to Robbrecht, 1988). sented as Appendix 3. The individual cells are not distinguishable from the Agepon for 12 h, fixed in Carnoy’s medium (96% ethanol/99% acetic acid, 3:l) and boiled for 10min in a 4% H202solution. Prior to observations the seeds were cleaned ultrasonically for a t least 1h and dried a t 80°C. Terminology follows Barthlott & Ehler (1977) and Stearn (1966). Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zy zyxwvutsr THE CHARACTERS AND THEIR STATES GROWTH FORM AND ECOLOGY Detailed information concerning the growth habit of Erectaria species is lacking. The following data are outline of the hairs (SEM observations) and the septa are much thinner than the outer wall. The optical active outer wall is c. 0.5 pm thick and both LM and SEM (Fig. 2) observations show that the wall is built up of many layers. The outer wall is ornamented by short or long cuticular striae (Fig. 1). 6 zyxwvutsr zyxwvut zyxwvutsrq S. DESSEIN ET AL. LEAVES AND STIPULES Leaf morphology The leaves of Virectaria are decussately arranged, and have a distinct petiole (except in X angustifolia and R salicoides). The blades are ovate (e.g. Xpmcumbens) to narrowly lanceolate (e.g. X angustifolia) and small or moderate in size (up to 15cm long and 8 cm wide). The leaf-blade apices are acute or somewhat rounded (Xpmcumbens, X belingana), their bases more or less acute. About 4-8 pairs of principal lateral veins are present. The lateral veins are not prominent and only slightly raised. Multicellular hairs are present on the primary and secondary veins of all species (Fig. 3) except R herbacoursi, where the long setose hairs are restricted t o the petiole and the leaf basis. Especially on the upper surface, the epidermis is papillose in X major, X multiflora and R belingana (Figs 5, 6). The stomata are restricted t o the lower surface of the lamina (hypostomatic) and are abundantly present on the leaf tips (upper third of the leaf). The stomata are of the paracytic type (Fig. 4), which is most common in Rubiaceae (cf. Wilkinson, 1979). Anisophylly can be found in all species, and is especially marked in R pmcumbens, but is not a diagnostic feature for the species because many specimens are not anisophyllous. Stipules The interpetiolar stipules are simple and triangular (R angustifolia, X belingana) (Fig. 7), or divided in two or three (seldom four) distinct lobes or setae from a short base (R multiflora, R tenella, V salicoides) (Fig. 8). Sometimes the stipules at the base of the plant are simple, while on the upper part they are divided (R major, X herbacoursi, R pmcumbens). The stipules of X herbacoursi are bent backward for more than 90". Colleters are present on the inner part of the stipules and more rarely on the tips of the setae. They correspond with the conical and stalked variant of the standard type of colleter in Rubiaceae (Robbrecht, 1988: Fig. BOA,B,E). Leaf anatomy Virectaria leaves are very thin in texture (80-120 pm). The radial walls of the rectangular epidermal cells are somewhat wavy, both above and underneath (Figs 4, 5). The cuticle is very thin. A hypodermis is absent. The mesophyll comprises only one or, more seldomly, two layers of pallisade parenchyma and one or two layers of loosely arranged spongy parenchyma; the distinction between these two types is not clear (Figs 6, 9). All mesophyll cells contain many large chloroplasts (Fig. 9). Collenchyma and sclerenchymatous tissues are totally lacking. The mesophyll is provided with numerous vascular bundles (Fig. 10). The main vein is fan-shaped, and is built up by 7-15 rows of tracheary elements (up to 5 cells high) and a more compressed phloem layer (Fig. 11).A single loosely arranged layer of large parenchymatous cells without chloroplasts surrounds all veins. Crystal sand with small spiny druses is abundantly present in the leaves of Virectaria. Narrow styloids were observed in X angustifolia (Nemba & Thomas 321). Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 The length of the hairs and the number of cells vary considerably between the different plant organs and between species. In X multifira two hair types are present on the stems: short, curved hairs, built up by a limited number of cells, and long (up to lmm), setiform hairs, which are built up by 30 and even more cells. The latter hair type is also found on the ovary, the stipules and the calyx lobes of this species and on the calyx lobes of X tenella and X herbacoursi. In X angustifolia only short, stiff setiform hairs are present. In all other species, short, curved hairs are found together with longer hairs, which seldom exceed 0.5 mm. The internal indumentum consists of unicellular, thin-walled hairs. The wall is optically inactive and the outside is beset with small warts. zyxwvu zy WOOD ANATOMY Growth rings are absent. Vessels are predominantly solitary, or rarely in radial multiples of 2 or 3 (Figs 12-14). The vessel outline is oval. Perforation plates are simple and the minute and vestured intervessel pits alternate. Vessel-raypits are similar t o intervessel pits in size and shape. Tangential diameter of vessel lumina is 40-(63h90 pin X major subsp. spathulata (Louis 10971) and 20-(28.5)40 pm in R major subsp. major (Lebrun 4242) and in R angustifolia. There are on average 60 vessels per mm2 in R major subsp. spathulata (Louis 10971), and >lo0 in the other two wood samples. The mean vessel element length is 350-(495)-640 pm. Tracheids and fibriform vessel elements with small simple perforations are common. Fibres with simple pits or reduced pit borders occur on radial fibre walls; septa were only sparsely observed in X major subsp. spathulata (Louis 10971). Fibres are 500-(660)-800 plong, thin-walled and very thinwalled in X major subsp. spathulata (Louis 10971). Axial parenchyma is absent. Rays are 2-3-seriate in X major subsp. major (Lebrun 4242), 4-5-seriate in X major subsp. spathulata (Louis 10971) and 1-2seriate in X angustifolia (Figs 15, 16). Rays are composed of upright and/or square ray cells; ray portions are often interconnected. The number of rays per mm zyx zy zy SURVEY OF VIRECTARIA 7 bract is often beset with colleters. At the lower part, the prophylls are larger, more or less leafy, and sometimes still possess short triangular or fimbriate stipular parts. Some other modifications and trends are observed in X major. Unequal development of the prophylls is clearly visible a t the lower nodes of the inflorescence: one of the prophylls is leafy, while the other is but a lanceolate tooth. At some nodes a single, small triangular prophyll is present, the other being totally reduced. The inflorescences of the other Erectaria species can be derived easily from the R major model by postulating the following trends: Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 17a I (1) Abortion of the terminal flower. Although the terminal flower is the first initiated, in most cases well developed, and the first to mature, in some cases it is aborted, resulting in a bifurcation of the inflorescence (Fig. 17C). (2) Shift of the bracts along the axes (Fig. 17D). zyxwvutsrq zyxwvut 17d i Figure 17. Scheme of inflorescences in Virectaria. A, central inflorescence type in Mrectaria. B, monochasial branching in upper part of inflorescence. C, bifurcated inflorescence due to aborted terminal flower. D, shift of bracts along the axes. (1) Impoverishment of the inflorescences. R p m cumbens, X tenella and X salicoides have pauciflorous inflorescences. (2) Additional inflorescences from the lower nodes. Such axillary inflorescences are common in R multiflora and R pmcumbens, but were also observed in other species. (3) Elongation of the axis during fruit maturation. This phenomenon is observed in some specimens of X multiflora, X herbacoursi and R tenella. In X multiflora, this results in a bilinear arrangement of the fruits. (4) Leafiness of prophylls in the whole inflorescence. This is present in some specimens of X angustifolia and X multiflora. zyxwvutsrq zyxwvu is more than 12. Ray height up to l m m or more. Mineral inclusions are absent. Wood of X major subsp. spathulata reveals several characters typical for climbing plants: wide vessels, broad rays and very thin fibre walls. INFLORESCENCE In Virectaria the inflorescences are terminal, determinate (i.e. the growing point of the inflorescence is transformed into a floral apex) and compound. The inflorescence of R major can be described as a multiflowered determinate thyrse (the central type of rubiaceous inflorescence according to Weberling, 1977), in which the main flowering axis is often immediately terminated with a flower (Fig. 17A). The branches originating in the axils of the prophylls follow the same branching pattern (i.e. the axillary branch ends in a flower, while new branches originate in the axils of the prophylls) and overtop the parent axis. At higher orders, the ramification continues from only one of the prophylls (the other prophyll is caducous) resulting in a monochasial branching pattern (Fig. 17B). The branches are very short and the flowers are subsessile. The prophylls are small and lanceolate or triangular in the upper part of the inflorescence. The base of the FLORAL MORPHOLOGY Flowers are homostylous and 4-8-merous. According to the information available on herbarium labels, scent seems to be lacking. Calyx The calyx tube is ovoid or urceolate, often bristly hairy. Sometimes the calyx consists of only the free calyx lobes (V rnultiflora). The 3-6 calyx lobes are equal (e.g. V pmcumbens) or unequal (e.g. X major var. spathulata);the shape varies from elliptic or lanceolate to filiform or spathulate (e.g. X procumbens). Some specimens of X multiflora have unequal leaf-like calyx lobes. Colleters are placed inside the calyx tube and at its margin, in the sinuses between the lobes. The ‘small appendages’ between the calyx lobes mentioned by Hall (1972) are in fact colleters; his morphological 8 zyxwvutsr zyxwvutsr S. DESSEIN ET AL. Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zyxwvutsr zyxwvu Figures 18-24. Floral morphology (SEM) of Mrectaria major subsp. spathuhta. Fig. 18. Tip of an inflorescence axis bearing two flower buds (their ovaries marked ‘ov’) with respectively (bud a t left) three and (bud at right) two enlarged calyx lobes (the fourth, small calyx lobe of left bud indicated by arrow). Fig. 19. Inside of corolla showing hairs at the base of the anthers. Fig. 20. Inside of corolla tube. Fig. 21. Anther. Fig. 22. Back-face of top of the anther with striated surface. Fig. 23. Young developing flower (outer parts removed) showing four anthers (the fifth removed) and two separated cones, of the young style and stigma. Fig. 24. Mature capitate stigma with papillate surface. zyxwvut explanation (reduced stipular segments) of these structures is not correct. Some specimens of X angustifolia and R major subsp. spathulata have h i t s crowned with only two or three equal calyx lobes. However, the young flower buds of these species possess four unequal calyx lobes of which one is aborted during maturation (Fig. 18). Calyx lobes of X herbacoursi and X tenella are crowned with one or two subapical setose hairs; R multiflora has many setose hairs. Comlla Corollas of Krectaria are small, white or pink to violet. The aestivation of the corolla lobes is valvate; a t the outside, the lobes are slightly concave, so that aestivation slightly tends to the reduplicate variant of valvate (Fig. 33). The corolla tube (4-17mm long) is narrow, filiform to infundibiliform. Usually the corolla tube is hairy; that of R herbacoursi var. herbacoursi is glabrous. Verdcourt (1953) stated that the throat is zyx zyx zyxwvuts zyxwvu SURVEY OF VIRECTARIA for the greater part naked, although there is a n obscure ring of non-septate hairs some distance below the orifice (Figs 19, 20). Although generally true, some specimens of X angustifolia and X pmcumbens lack such a ring. Like most Rubiaceae the hairs of the internal indumentum are unicellular. The 4-6 (7-8 for X belingana) corolla lobes are deltoid to lanceolate. Gynoecium The glabrous style ends in a truncate, swollen stigma (Fig. 24). Ontogenetically the style is developed by the postgenital adnation of two separated cones (Fig. 23). The stigma initially consists of two lobes beset with papillae (or short hairs) but these lobes are invisible in the full-grown stigma, which is spherical and covered with rounded papillae. The ovary is bilocular; each locule contains a peltate placenta, sitting on a broad and short stalk attached from the base up to the middle of the septum (Figs 26, 27, 29). Cross sections of the placenta reveal that the upper part of the septum consists of two thickened parts in the centre of the ovary which are partly fused (Fig. 37). At the lower half of the septum the two parts are fused and boundaries cannot be observed (Figs 38, 39). This placenta type can be derived from the Ushaped type (cf. De Block & Robbrecht, 1997) by reduction of t.he stalk and a further outgrowth of the septum in the upper part of the ovary. Crystal sand is abundantly present in the cells of the placenta, the septum, and the nectary disc (Fig. 40). The tenuinucellate and unitegmic ovules develop in a sequential order on the placenta, starting a t the top (Figs 25, 26, 36) (cf. similar observation in Mussaendopsis, Puff & Igersheim, 1994). The massive integument surrounds the nucellus and the megaspore mother cell, which develops into the embryo sac. At the youngest stages, however, the nucellus protrudes from the micropyle (Fig. 30). The eight-nucleate embryo sac contains starch grains, a common condition in Rubiaceae. In a later stage, the young ovules partly overlap each other and the micropyle is orientated downwards (Fig. 31). In the competition for space, some ovules are aborted but remain attached to the placenta like small pieces between the developing seeds (Figs 28, 32). The full-grown ovules are more or less campylotropous and irregularly angular. Three of the eight species (R multiflora, X herbacoursi and X tenella) possess a disc on top of the ovary, which is split in two narrow bilobed parts (Fig. 45). The whole epidermal surface is covered with papillae; nectarostomata seem to be absent (Fig. 46). The five other species have a massive, cylindrical disc (Fig. 41). It is borne on the upper part of the ovary as a continuous waving girdle surrounding the stylar base. The full-grown disc is very prominent and can be more than 0.8 mm tall. The apex is somewhat wavy or slightly 3-5 lobed (Fig. 42). Nectarostomata are present on the upper part (Figs 42, 43). Cross sections of X major reveal tanniniferous idioblasts throughout the central part of the disc (Figs 35, 44). FRUIT MORPHOLOGY AND ANATOMY Virectaria fruits are globose or ellipsoidal bilocular capsules. The young hairy fruits (Fig. 47) are crowned with the calyx lobes and the beak (remnants of the nectar disc). The fruit wall is built up by three distinct layers (Fig. 48). The locule first opens a t the apex (Fig. 49); later the opening extends to the upper half (Fig. 50). During dehiscence, one valve of the capsule drops off while the other remains attached to the pedicel (Figs 51, 52). The loculicidal opening is sometimes incomplete. Therefore, the valves remain attached to the pedicel and to each other (e.g. common in X major). In X pmcumbens and X angustifolia and some specimens of X multiflora, the attached part rolls up (Fig. 52). The opening of the fruit of Virectaria into one persistent and one caducous valve is typical for the genus and unique in Rubiaceae. The different behaviour of the two parts might well have a function with regard to partitioning seed portions for short and long distance dispersal, as it occurs in many angiosperms. Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 And meciu m The anthers are exserted, narrowly lanceolate and with two thecae with two pollen sacs each, opening by longitudinal slits (Figs 21, 34). The anthers are dorsimedifixed and the epidermis is distinctly striate (Fig. 22). The glabrous filaments are attached near the top of the corolla tube, due to postgenital adnation. 9 zyxwvuts SEED MORPHOLOGY AND ANATOMY Seed morphology Virectaria seeds are small (up to 600 pm long, 500 pm broad and 350 pm high) and angular; in general they have the shape of a knotted pyramid; sometimes they are more prismatic (Figs 53-55). The hilum (often forming a small depression) is situated a t the smallest surface of the seed (Figs 54,55). The mature seeds are brown and their surface has a reticulate pattern. The exotesta cells are angular and elongated (e.g. R herbacousi, on average 95 x 40 pm) or strongly elongated (e.g. V: major, on average 100 x 18 pm) (Figs 57-59). Seed anatomy The seed coat is exotestal. The parenchymatous endotesta is completely collapsed and hardly visible in 10 S. DESSEIN ET AL. Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 F igures 25-32. Placentation (SEM) of Virectaria major subsp. spathulata. Fig. 25. Young placentas attached to the septum. Fig. 26. Two placentas showing developing ovule primordia. Fig. 27. Placentas with overlapping ovules. Fig. 28. Placenta with very young seeds and aborted ovules, outer view. Fig. 29. Inside of placenta showing insertion place of the broad stalk. Fig. 30. Young stage of developing ovule, showing the initiation of the single integument. Fig. 31. Older stage of ovule. Fig. 32. Detail of an aborted ovule surrounded by larger, fertile ovules. transverse sections of mature seeds. The exotesta has conspicuous verrucate to tuberculate thickenings on the radial walls and often also on the inner tangential wall (Figs 57-60). In the angles of the exotesta cells, these thickenings are prominent. The outer tangential wall lacks secondary thickenings, except for V. tenella and V. herbacoursi, were the outer wall is granular in appearance (Fig. 59). In seeds treated with H 20 2 the outer tangential wall readily disappears so that the secondary thickenings become visible in SEM surface zyx z SURVEY OF VIRECTARIA 11 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zyxwvuts zyxwv z zyxwvuts Figures 33-40. Floral morphology and anatomy (LM) of Virectaria major subsp. major. Fig. 33. Cross-section through top of flower bud showing valvate aestivation of corolla lobes. Scale bar = 200 pm. Fig. 34. Cross-section of anther. Scale bar = 200 pm. Fig. 35. Cross-section through basis of flower bud showing from inside to outside: style, disc, corolla, colleters, and calyx lobes. Scale bar =200 pm. Fig. 36. Longitudinal section (LS) of young ovary showing the most far developed ovules at top of placenta. Scale bar=200 pm. Fig. 37. Cross-section of upper part of ovary revealing the partly fused thickened parts of the septum. Scale bar = 200 pm. Fig. 38. Cross-section of middle of ovary showing broad and short stalk of placenta. Scale bar = 200 pm. Fig. 39. Cross-section of lower part of ovary showing continuous septum. Scale bar = 200 vm. Fig. 40. LS ovary showing crystal sand in septum, placenta and nectar disc (the illuminated sections contain crystal sand). Scale bar =200 pm. views. The secondary thickenings are mostly smooth, but those of X tenella and X herbacoursi are covered with a fine and dense puncticulate pattern (Fig. 60). Small pores perforate the inner tangential wall (Figs 58,60). At the endosperm side of the inner tangential wall, each pore is surrounded by a narrow ridge (Fig. 12 S. DESSEIN ET AL. Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Figures 41-46. Features of nectary disc (SEM except 44, LM) in Virectaria. Fig. 41. V. major subsp. major: ringlike nectary disc on top of ovary. Fig. 42. V. major subsp. major: detail of top of nectary disc showing nectarostomata. Fig. 43. V. major subsp. major: detail of a nectarostoma. Fig. 44. V. major subsp. major: cross-section of disc showing tanniniferous idioblasts in disc tissue. Scale bar= 20 Jilll. Fig. 45. V. multi/lora: deeply bipartite disc on top of ovarium. Fig. 46. V. multiflora: detail of surface of bipartite disc. 56). The function of these pores is still unknown, but they might play a role in rehydration of the seed. The horny endosperm surrounds the relatively large embryo, which attains c. a third of the length of the seed. POIJ.EN Huysmans, Robbrecht & Smets (1998) provided pollen morphological information of V. 1nultiflora and V. procumbens. We have examined all other species except V. salicoides and V. tenella. zyx zy SURVEY OF VIRECTARIA 13 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zyxwvuts zyxwvuts zyxwv zyx zyxwvutsrqp Figures 47-52. Fruit features (SEM) of Virectaria. Fig. 47. V pmurnbens: closed fruit with the persistent spathulate calyx lobes. Fig. 48. X major subsp. major: cross-section of fruit wall. Figs 49, 50. V multiflora:early and later stage of apical-loculicidefruit dehiscence (se=septum, nd=remnants of nectary disc). Fig. 51. V angustifolia: top view of the fmit part that remains attached t o the pedicel; the second valve dropped off. Fig. 52. V angustifolia:side view of the attached, enrolled fruit valve. Pollen grains of Erectaria are 3-colporate (Fig. 62) and medium sized (average P-values vary between 4 5 . 2 ~ in X angustifolia and 34.9pm in V herbacoursi, and E-values between 33.0 pm in V belingana and 25.4 pm in R herbacoursi). Their shape in equatorial view is prolate to subprolate ( X p m u m b e n s : P/ E = 1.10 and V multiflora:P/E = 1.15) or prolate (other species: average P/E-values vary between 1.36 and 1.41; Fig. 61). The ectoapertures are colpi with acute, or somewhat rounded ends (Fig. 64), and the ectoaperture width varies from 1.6 pm in X angustifolia to 3.5 pm in X major. The colpus membrane is more or less granular (Fig. 63). X herbacoursi and R pmcumbens have a colpus membrane that is beset with large granules arranged in a central row. The mesoaperture lacks any differentiation and appears as a gap in the colpus membrane; sometimes it is surrounded by a n annulus 14 zyxwvutsr zyxwvutsrqpon zyxwvutsrq zyxwvuts S. DESSEIN ET AL. Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zyxwvu zyxw Figures 53-60. Seed morphology and seed anatomy (SEM) of Erectaria. Fig. 53. R angustifolia: adaxial view of seed surface (treated with acids). Fig. 54. V tenella: abaxial view of seed surface showing hilum (untreated seed). Fig. 55. R major subsp. major: abaxial view of seed surface showing hilum (treated with acids). Fig. 56. V major subsp. major: endosperm side of inner tangential wall of exotesta (treated with acids). Fig. 57. V major subsp. major: detail exotesta (untreated). Fig. 58. R major subsp. major: detail exotesta (treated with acids) showing verrucate thickenings on radial walls and perforations of inner tangential wall. Fig. 59. V tenella: detail exotesta (untreated) showing coarsely outer tangential wall. Fig. 60. V tenella: detail exotesta (treated with acids) showing perforations of inner tangential wall and very small granules on inner walls of exotesta. SURVEY OF VIRECTARIA 15 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Pollen morphological features (SEM) in Virectaria. Fig. 61. V major subsp. major: equatorial view of Figures 61~. prolate pollen grain. Fig. 62. V herbacoursi: polar view of pollen grain. Fig. 63. V major subsp. major: detail equatorial view showing ecto· and mesoaperture, and central row of granules on colpus membrane. Fig. 64. V major subsp. major: detail polar view showing rounded ectocolpus ends. Fig. 65. V major subsp. major: detail perforate tectum. Fig. 66. V angustifolia: detail sexine showing curved, smooth sexine elements on top of perforate tectum. Fig. 67. V major subsp. major: inside of broken pollen showing granular nexine and H-shaped endoaperture. Fig. 68. V herbacoursi: inside of broken pollen grain showing small endocolpus with acute ends, perpendicular on ectocolpus. zyxwvutsrq zyxwvutsrq zyxwvut zyxwvutsr zyxwvuts zyxwvut zyxwvutsrqp 16 S. DESSEIN ETAL. (Fig. 63). A small endoaperture is present (Fig. 68), which is sometimes H-shaped (Fig. 67). The sexine has perforations smaller at the poles than in the mesocolpia (Fig. 65). The tectum of X pmcumbens and X angustifolia is beset with elongated and curved or more rounded sexine elements (Fig. 66), which are always smooth (cf. Huysmans et aL, 1998). The inner nexine surface is granular. KARYOLOGY 5N 0 GEOGRAPHICAL DISTRIBUTION Erectaria is limited to tropical Africa, and is an essentially Guineo-Congolian wide genus. White (1979) divided the Guineo-Congolian Region into three subcentres of endemism (for which we use the term Domain, cf. p. €9, i.e. Upper Guinea, Lower Guinea, and Congolia. V multiflora and V p m u m b e n s have similar distributions in the Guineo-Congolian Region (see Fig. 70B,C), except that the latter is less well represented in the eastern Congo. The two species are absent, or almost absent, from the parts of the Congo Basin below 500 m (i.e. the area between 18”Eand 25”E and between 2”N and 3”s). V major subsp. major is also widespread, but is limited to higher altitudes, ranging from 800m to 2800m (Fig. 70A). It cannot be considered as a strict Afromontane species, because of its presence in places not usually considered mountain ranges; the species extends to the Zambezion Region and the Lake Victoria regional mosaic. V major subsp. spathulata is centred in the Congolian Domain. It has a disjunct element in Cameroon (Lower Guinea) and a markedly disjunct element in the Upper Guinea Domain (Fig. 70A). X major subsp. decumbens is a narrow endemic of Zambia. Four species are endemic to Lower Guinea: X herbacoursi (reported from Cameroon and Gabon; Fig. 69C), V belingana (reported from Cameroon and Gabon; Fig. 69B), V salicoides (restricted to Gabon; Fig. 69D), and V angustifolia (reported from Cameroon and Gabon; Fig. 69A). One species is endemic to Upper Guinea: I? tenella (Ghana only; Fig. 69C). The ‘coincidence map’ (Fig. 70D) reveals well-known ‘hot spots of endemism’ as Gabon (5 taxa) and southwest Cameroon (5 taxa). 1OW 5W 0 5E 10E 15E 20E Figure 69. Distribution maps of species of Virectaria. A, V angustifolia (var. angustifolia = + ; var. schlechteri = 0).B, I? belingana.C, ?% tenella (= 0 )and R herbacoursi (var. herbacoursi = +, var.petmphila = +).D, R salicoides. VERNACULAR USE X major is frequently used in traditional medicine (cf. Baerts & Lehmann, 1989, 1991; Burkill, 1997). It is utilized to heal all kind of disorders, varying from eye diseases to pneumonia. Most collectors report that decocted leaves are used for healing wounds, which is reflected in the Mahi vernacular name “Kalyabirondo” (Congo), signifying “that which eats wounds”. TAXONOMIC TREATMENT Four taxa were described after Verdcourt’s (1953) revision of the genus. The present survey of the genus confirms their status as distinct species. It is useful to summarize the specific and infraspecific differences in a key to all taxa (Table l), and to give a brief taxonomic survey of the genus. TAXONOMIC SURVEY Erectaria Bremek. Verh. Kon. Ned. Akad. Wetensch., afd. Natuurk., Tweede Sect. 48(2): 21 (1952). Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Kiehn (1995) provided the only report of chromosome numbers for the genus Virectariu. R pmcumbens of West Africa is tetraploid with a basic chromosome number X = 10. This single count was considered as an additional argument for excluding Wrectaria from the Rondeletieae (Kiehn, 1995). z zyxw SURVEY OF WRECTARIA Habitat. Rocky banks in river. 17 Distribution. Gabon, Cameroon, and South Nigeria (Fig. 69A). var. schlechteri Verdc., Bull. Jard. Bot. Etat Brux. 23: 48 (1953). 10 N zyxwvutsrqp 0 Type. Cameroon, Schlechter 12926 (BR, holo). 10 s Habitat. Rocky banks in river. zyxwvutsr Distribution. Cameroon (Fig. 69A); only known from type. 10 N Erectaria belingana N.Halle, F1. Gabon, 12234 (1966). Type. Gabon, Belinga, Halle 2799 (P, holo). 10 s Habitat. Rocky places. Distribution. Gabon & Cameroon (Fig. 69B). 10 N Note. The specimens collected in Cameroon have slightly larger leaves, and the branches are less divaricated. The calyx lobes, however, are minute as in V belingana. 0 10 s Erectaria herbacoursi N.Halle, FZ. Gabon, 12: 88 (1966). 10 N 0 Type. Gabon, entre Mbigou et Lebamba, Halle & Cours 6177 (P, holo). var. herbacoursi: N.Halle, F1. Gabon, 12: 88 (1966). Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 0 zyxwvutsrqpon zyxwvuts zyxwvuts 10 s 21 Figure 70. Distribution maps of species of Mrectaria. A, I? major (subsp. spathulatar 0 ;subsp. major= +; supsp. decumbens=+). B, V multiflora. C , V procumbens. D, coincidence map of infraspecific taxa. Habitat. Meadow on laterite soil. Distribution. Gabon (Fig. 69C). var. petmphila N.Halle, FZ. Gabon, 17: 2 (1970). Type. Cameroon, Mildbraed 5543 (HBG, holo). Synonyms. Erectaria petmphila Mildbr. (nomen). Synonyms. Krecta Afzel. ex Sm. in A.Rees, Cycl. 37: 2 (1818); Phyteumoides Smeathman ex DC., Prodr. 4: 414 (1830). Habitat. Meadow on laterite soil. Erectaria angustifolia (Hiern) Bremek., Verh. Kon. Ned. Akad. Wetensch., afd. Natuurk., Tweede Sect. 48(2): 21 (1952); Verdcourt, Bull. Jard. Bot. Nut. Be%. 23: 35-52 (1953); Hepper, R W T A . , ed.2, 2: 209 (1963); N. Halle, Fl. Gabon, 12: 82 (1966). Erectaria major (K.Schum.) Verdc., Bull. Jard. Bot. Etat Brux. 23: 42 (1953); Hepper, R W T A . , ed. 2, 2: 208 (1963); F1. P1. Lign. Rwanda: 612, fig. 208/1(1982); Fl. Rwanda 3: 230, fig. 74/1 (1985); F1. Tmp. E. AfK, Rubiaceae2: 458, fig. 68 (1988). Type. Ivory Coast, 1" lat. N, Monts de Cristal, Mann 1686 (K, holo). Type. Tanzania, Bukoba, Sthulmann s.n. (B, holo; +). Synonyms. cf. Halle (1966). var. angustifolia: Bremek., Verh. Kon. Ned. Akad. Wetensch., afd. Natuurk., Tweede Sect. 48(2): 21 (1952). zyxwvu Distribution. South Cameroon (Fig. 69C); narrow endemic. Basionym and synonyms. cf. Verdcourt (1988). Note. The most widely distributed and most variable species of the genus. We here adopt the infraspecific zyxwvutsr zyxwvuts zyxwvut zyxwvu zyxwvutsrq 18 S. DESSEIN ET AL. KEY TO SPECIES AND INFRASPECIFIC TAXA * The specimens collected in Southeast Congo are somewhat different from other specimens included in subsp. spathulata. Although their calyx lobes are distinctly spathulate, they differ in having smaller leaves, being more or less erect herbs and in the characteristics of the indumentum. Field observations and additional material are needed to clarify the position of these specimens. taxa based on calyx morphology proposed by Verdcourt (1953), but found that his two varieties in subsp. major are also distinguishable by their habit and inflorescences (robust habit and very dense inflorescence in var. major, slender to lianescent habit and a tendency to more lax inflorescences in var. spathulata). Because the morphological distinction is correlated with distributional and ecological differences (var. major: predominantly montane grasslands; var. spathulata: predominantly lowland forests) it is better to recognize them as subspecies. Some special forms of subsp. spathuZata occur in South-West Congo (cf. supra). Subspecies decumbens was described by Verdcourt (1993), and is a n endemic of Zambia. subsp. major. Habitat. Moist upland grassy places, more seldom border forest. Distribution. Bioko, Burundi, Cameroon, Congo, Ni- geria, Rwanda, Tanzania Uganda, Zambia (Fig. 70A). subsp. spathulata (Verdc.) Dessein & Robbr. stat. nov. Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Disc entire; long setose hairs absent on calyx lobes .............................................................................................. 2 Disc divided into 2 cones; 1 to many setose hairs present on calyx lobes ........................................................... 9 Small subshrub with rheophytic adaptations; leaves narrow (<1.2 cm wide) ..................... Straggling or erect herb; most leaves broader than 1.2 cm .................................................................. Corolla tube less than 0.5 mm long; inflorescence few-flowered; stipules undivided .......... Corolla tube more than 0.5 mm long; inflorescence many-flowered; stipules with 2-3 setae or lobes, sometimes simple a t the lower nodes ...................................................................................................................... X salicoides Leaves narrowly elliptic or oblanceolate, 3.7-5cm long and 0.65-1.2cm wide, bluntly pointed at the apex ...... ........................................................................................................................ V angustifolia var. angustifolia eaves oblong-lanceolate, 2.9 cm long and 0.5 cm wide, rounded a t the apex ... R angustifolia var. schlechteri Erect herb or subshrub, or decumbent herb exceeding 0.5 m; corolla tube longer than 0.7 mm, inflorescence many or few-flowered ............. ........................................................................................ 6 Straggling herb, not exceedi la tube shorter than 0.7mm; calyx lobes short a lY spathulate; inflorescence few-flowered, attached fruit part rolling up; anisophylly often present ........................ .............................................................................................................................................................. X pmcumbens Inflorescences many-flowered; stipules with 2-3 setae or lobes, sometimes simple at the plant’s base; calyx lobes long ................................................................................................................................................................... 7 Inflorescences few-flowered; stipules mostly undivided; plant with divaricate branching; calyx lobes short ...... ................................................................................................................................................................. R belingana Habit erect up to 3m tall; calyx lobes filiform or spathulate ......................................................................... Habit more or less decumbent, c. 0.75 m long, calyx lobes spathulate .................... R major subsp. &cum bens Habit more or less climbing; plant with long and somewhat curved internodes; inflorescences tending to be lax, especially in fruiting stage; calyx lobes often unequal, and often spathulate ........ R major subsp. spathulata* Habit erect; plant with short, straight internodes; inflorescences condensed; calyx lobes equal or unequal, all filiform ....................................................... ..................................................................... X major subsp. major Inflorescences many-flowered;plant abundantly covered with spreading hairs; annual erect herb, often somewhat woody a t the base .................................................................................................................................. X multiflora Inflorescences few-flowered; plant glabrous or sparsely pubescent; straggling herbs, sometimes with erect branches ............................................................................................................................. .................. 10 Corolla tube less than 8mm long; calyx lobes deltoid or foliaceous - spathulate; present; leaves small ( 4 5 mm long) .................................. .................................................................. X tenella Corolla tube more than 8mm long; calyx lobes linear; hairs on external corolla absent or sparsely present; leaves more than 15mm long ................................................................................................................................ 11 Ovary and corolla glabrous, one subapical setose hair on calyx lobes ............... X herbacoursi var. herbacoursi Ovary and corolla sparsely pubescent, two subapical setose hairs on calyx lobes ................................................. .................................................................................................................................... X herbacoursi var. petrophila zyx SURVEY OF VIRECTARIA Type. Congo (Kinshasa), Kasongo, Claessens 551 (BR, holo). Type. Unknown. 19 Basionym and synonyms. cf. Halle (1966). Basionym. Erectaria major var. spathulata Verdc., Bull, Jard. Bot. Etat Brux. 23: 46 (1953). Habitat. Wet places, often along rivers; more seldom epiphytic (e.g. on Baillonella toxisperma). Habitat. Lowland forest, more seldom wet grasslands. Distribution. Bioko, Cabinda (Angola), Cameroon, Congo, Congo (Braz), Equatorial Guinea, Gabon, Ghana, Guinea, Ivory Coast, Liberia, Nigeria, Sierra Leone (Fig. 70C). Note. We consider that some of the material named var. major by Verdcourt (1953) is better placed in subsp. spathulata - these specimens are indicated with an asterisk in appendix A. subsp. decuinbens Verdc., Bull. Jard. Bot. Belg. 62: 415 (1993). Type. Zambia, Mungwi, Robinson 4018 (K, holo). Habitat. Grassland, along river. Erectaria salicoides (C.H. Wright) Bremek., Verh. Kon. Ned. Akad. Wetensch., Afd. Natuurk. Tzueede Sect. 48(2): 21 (1952);Verdcourt, Bull. Jard. Bot. Etat Brux. 23: 49 (1953); N. Halle, F1. Gabon, 12: 84 (1966). Qpe. Gabon, Bates 527 (K, holo). Basionym and synonyms. cf. Halle 1966. Habitat. Rocky banks by river. Distribution. Narrow endemic to northern Zambia (Fig. 70A). Distribution. Endemic in Cristal Mountains, Gabon (Fig. 69D); only known from type. Erectaria lrLultifEora (Sm.) Bremek., Verh. Kon. Ned. Akad. Wetensch., Afd. Natuurk. Tweede Sect. 48(2): 21 (1952); Verdcourt, Bull. Jard. Bot. Etat Brux. 23: 40 (1953); Hepper in RW.TA., ed. 2, 2: 208 (1963); N. Halle, in Fl. Gabon, 12: 87 (1966). Erectaria tenella J.B.Hal1, Kew Bull., 26: 569 (1972). Type. Ghana, Gbadzeme near Amedzofe, Botokro & Hall 40011 (K, holo). Type. Sierra Leone, Afzelius s.n. (BM, holo). Habitat. Shaded low vertical cliff with bedded siliceous rocks whose cracks remain moist. Synonyms. cf. Halle (1966). Distribution. Ghana (Fig. 69C). Habitat. Grasslands, inundated wet places, granitic slopes of rocky hills, ruderal terrains. Distribution. Cameroon, Cabinda (Angola),Central African Republic, Congo, Congo (Braz), Equatorial Guinea, Ghana, Guinea, Guinea Bissau, Ivory Coast, Liberia, Nigeria, Senegal, Sierra Leone (Fig. 70B). Note. A widely distributed and quite variable species (e.g. corolla tube size ranging from 5mm to 1Omm; calyx lobes linear or unequal leaf-like, leaves elleptic or lanceolate), but the variation is too unordered to allow recognition of infraspecific taxa. Erectaria pmcumbens (Sm.) Bremek., Verh. Kon. Ned. Akad. Wetensch., Afd. Natuurk. Tweede Sect. 48(2): 21 (1952); Verdcourt, Bull. Jard. Bot. Etat Brux. 23: 46 (1953); Hepper in R N T A . , ed. 2, 2: 208 (1963); N. Halle, F1. Gabon, 12: 80 (1966). DISCUSSION Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zyxwvutsrq zyxw Distribution. Cameroon, Central African Republic, Congo, Ivory Coast, Liberia, Sierra Leone (Fig. 70A). zy zyxw RELATIONSHIPS BETWEEN THE SPECIES OF VIRECTARIA Twenty-one characters were found significant for a n analysis of the relationships between the Erectaria species. The characters and character states recognized are summarized in Appendix 2. Tamridaea capsulifera was used as outgroup since molecular data support the relationship between this recently erected genus and Erectaria (Bremer & Thulin, 1998). Moreover, a second analysis with a hypothetical ancestor as outgroup was also made. Both analyses resulted in the same cladogram (Fig. 71: length 31, c.i. 0.806, r.i. 0.806). B salicoides was excluded from the analyses because both pollen and seed observations were lacking. Two clades can be recognized within the genus Erectaria. The first clade (bsu 4, bootstrap value 89), 20 zyxwvutsrqp zyxwvutsrq zyxwvuts , S. DESSEIN ET AL. V: angustifolia Vprocumbens TAXONOMIC POSITION OF VIRECTARIA As documented in the taxonomic history of the genus, the position of Virectaria in the Rubiaceae has been discussed at length. The genus has been associated with the Hedyotideae, Ophiorrhizeae, Pomazoteae, Rondeletieae, Sabiceeae s.1. and Sipaneeae. Verdcourt (1958) and Robbrecht (1988) previously discussed the exclusion of Virectaria from the Pomazoteae and Urophylloideae. Its position in the Sabiceeae (i.e. away from the Hedyotideae and Ophiorrhizeae), as recently proposed by Bremer & Thulin (1998), has drawn o u r attention and needs the following comments. A first question - whether Virectaria should be excluded from the subfamily Rubioideae - is now resolved. When placed in the Rubioideae, Wrectaria was associated with either the Ophiorrhizeae or Hedyotideae. Virectaria resembles these two tribes in its herbaceous growth habit, multi-ovulate placenta and dry fruits (Table 1). The similarity between R p m cumbens and Parapentas setigera (member of Hedyotideae) was so striking that r! setigera was included in Virectaria for a long time. There are, however, three major reasons for excluding the genus from the Rubioideae and for rejecting any affinity with the Ophiorrhizeae and Hedyotideae. Firstly, molecular evidence (e.g. Bremer, 1996) clearly supports Bremekamp’s and Verdcourt’s vision (Bremekamp, 1952, 1968; Verdcourt, 1958) on the importance of raphides as a diagnostic feature for the subfamily Rubioideae. The main morphological evidence for excluding Virectaria from the Rubioideae is the absence of raphides. Secondly, the seed anatomy of %rectaria differs strongly from the common seed exotesta type found in the Hedyotideae. Within the Hedyotideae two types of exotesta can be recognized (Dessein et al., in prep.). The first type, restricted to the so-called ‘Pentas group’ (cf. Bremer, 1987), has a puncticulate outer tangential wall and reticulate thickened inner walls. The ‘Oldenlandia group’ (cf. Bremer, 1987) on the other hand has Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 disc, the absence of long setose hairs, and the simple stipules (except for R major). R major is the basal species within the clade. R belingana is closely related t o R major, it resembles the latter in its growth habit, the presence of a papillous leaf epidermis and the large size of flowers. It differs in the smaller leaf size and the divaricate branching of the plant. Similar t o R major, R belingana, Kpmcumbens, and R angustifolia, R salicoides has an entire disc and long setose hairs are absent. Like R major, it shows divided stipules. It shares a rheophytic habit with R angustifolia to which it is closely related. It is possible that the species are sympatric, R salicoides being a polyploid from R angustifolia (cf. Verdcourt, 1953). zyxwvut zyxwvuts ‘ Tamridaea capsulifera Figure 71. Most parsimonious tree, figure above branch denotes bootstrap value, figure beneath branch denotes Bremer support for that branch. which comprises R herbacoursi, R tenella and R multiflora, is characterized by the deeply bipartite disc, the presence of long, patent multicellular setose hairs on the calyx lobes, the divided stipules, the relatively broad exotesta cells and the smaller pollen grains. R herbacoursi and R tenella form the sister group of R multiflora. They share puncticulate secondary thickenings on the radial walls of the exotesta, granular outer tangential walls of the exotesta, small fruits and reduction in number of fertile ovules. They differ from each other mainly in their growth habit; ‘c! herbacoursi is a creeping herb with robust erect branches, while R tenella is a slender, prostrate herb, without erect stems and with small inflorescences. Hall (1972) concluded therefore that the species were not closely related. We suggest, however, that this variation is caused by the specific ecology of ‘c! tenella, i.e. shaded low vertical cliffs, with bedded siliceous rocks whose cracks remain moist. Both species are narrow endemics: R tenella is known only from two populations in Ghana; while R herbacoursi is endemic to Gabon. The close relationship between these species is an example of a vicariant couple in Lower-Guinea and Upper-Guinea. The second clade (bsu 2, bootstrap value 63), including I? major, R angustifolia, R belingana, R p m cumbens, is characterized by the presence of an entire zy zyx z zyxwvuts zy zyxwvut SURVEY OF VIRECTARIA 21 Table 1. Summary of main morphological and anatomical features for Erectaria and possibly related groups, (O.T.W. = outer tangential wall, I.T.W. =inner tangential wall; R.W. =radial wall) Character M rectaria Ophiorrhiza- Hedyotideae Spiradiclis S.S. Sipaneeae Sabiceeae herbssubshrubs herbs-shrubs herbssubshrubs herbs lianas Stipules Inflorescence position entire or bifid terminal fimbriate terminal fimbriate terminal o r axillary entire or bifid terminal entire axillary Heterostyly absent present present present present Aestivation valvate valvate valvate contorted valvate Number of ovary locules 2 2 2 2 2-5 Sexine perforate reticulate reticulate (seldomly perforate) reticulate reticulateperforate Apertures colporate colporate colporate colporate colporate or pororate Seed morphology prismatic prismatic irregular angular prismatic, flattened prismatic Wings absent absent absenvpresent absent absent Exotesta cells strongly elongated elongated elongated isodiametricelongated strongly elongated Secondary thickenings on the O.T.W. absent absent present absent absent Thickenings R.W. or I.T.W. verrucate verrucate reticulate verrucate reticulate bands, often with warts Perforations on the I.T.W. pores small pores absent large pores large pores Fruit dehiscence loculicide, only one valve attached loculicide, loculicide and septicide loculicide and/ or septicide loculicide indehiscent Raphides absent present present absent absent a very reduced exotesta, with only the outer wall punctate or puncticulate. The seed anatomy of Virectaria resembles Spiradiclis and Ophiorrhiza in the unthickened outer tangential wall a n d the verrucate thickenings, but the perforations are much smaller, there are no thickenings at the angles of the exotesta cells, a n d the cells are isodiametric a n d not elongated. Finally, the simple stipules of Virectaria tend to indicate a position remote from the Hedyotideae a n d Ophiorrhizeae, because simple stipules are rarely found in either of these tribes. However, some genera, at present in the Hedyotideae, do have entire stipules (e.g. Sacosperma) but their position is disputed. The next question - which genera can be considered close relatives to Virectaria? - is more difficult to answer. Based on molecular evidence, Bremer & Thulin (1998) suggested a position near Tamriduea capsulifera, within the redefined tribe Sabiceeae. Bremer & Thulin (1998: 85) stated that: “there are several morphological traits that support an affinity between Virectaria a n d Tamridaea and their relationship to Sabicea and Pseudosabicea”. I n our opinion, however, this morphological support is r a t h e r weak. Tamridaea, Mrectaria, Sabicea a n d Pseudosabicea have only the valvate aestivation a n d some characteristics of the exotesta cell structure in common (see below). The dry fruit and its aberrant dehiscence, and the herbaceous growth habit of Erectaria do not fit the character states of Sabicea and Pseudosabicea. The morphological support for a close relationship between Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Growth form 22 zyxwvutsrqp zyxwvutsrq zyxwvut S. DESSEIN ET AL. lbmridaea capsulifera and Krectaria is also weak Erectaria differs from lhmridaea in the herbaceous growth habit, the floral morphology (homostylous with exserted stamens), the truncate stigma, the prominent nectar disc, the fruit dehiscence and the pollen morphology. Nor was the inclusion of Krectaria in the Sabiceeae supported by the palynological study of Huysmans et al. (1998). In their cladistic analyses based on pollen characters, Wrectaria formed a clade with the neotropical Raritebe (a genus with an uncertain position, and not included in the study of Bremer & Thullin, 1998). The two genera share features such as prolatespheroidal pollen grains with a perforate sexine and acute edocolpi. Huysmans et al. (1998) concluded that Erectaria and Raritebe belong to another alliance rather than to the Sabiceeae. Their Peewee analysis suggested Gonzakzgunia, the Mycetia/Myrwneumn complex or Gouldia (four genera included in the Isertieae by Robbrecht, 1988) as possible relatives. A character that has been overlooked in the discussion of the tribe Sabiceeae is the nature of the internal indumentum. Verdcourt (1958: 222-224) examined the trichomes of many Rubiaceae and distinguished two groups: the internal indumentum (inside the corolla) and the external indumentum (other plant organs). While Verdcourt (1958) considered the hair structure of the external indumentum as a useful secondary character, the systematic importance of the inner indumentum has never been discussed in the literature. The inner indumentum mostly consists of unicellular thin-walled trichomes, which are flat and ribbon-like or sometimes moniliform. The hairs of Sabicea and Pseudomussaenda capsulifera (= Tamridaea) were described as ‘constricted by Verdcourt (1958). The constricted segments are often wider than long, particularly at the distal end of the hairs. In Tamridaea, these constrictions are only present at the distal end. Our investigations confirm the presence of this type of hairs in Tamriduea and Sabicea and we also found them in Pseudosabicea and Ecpoma, but not in Erectaria, Mussaendu and its closest allies (Pseudomussaenda, Schizomussaendu). This type of constricted hairs is also found in Bertiera (Gardenieae) and some Psychtria (Psychotrieae) species (e.g. E! kirkii). The presence of constricted hairs strengthens the position of Tamridaea near Sabicea and its allies, but it indicates a more isolated position for Erectaria. Additional evidence for the isolated postion of Virectaria is found in the seed structure of the genus. Shape, seed size, size of the elongated exotesta cells, perforation density and dimensions of the inner tangential wall and shape of the verrucate thickenings are comparable within Sabicea, Pseudosabicea, Ecpoma and Tamridaea. Although, at first sight, Virectaria resembles this seed type, its seeds are smaller, their shape is more or less prismatic, the elongated exotesta cells have smaller perforations and there are prominent thickenings in the angles of the exotesta cells. In conclusion, we confirm that some morphological characters (e.g. constricted hairs and seed anatomy) strenghten the position of Tamridaea in the Sabiceeae, but exclude Krectaria. Another tribe sometimes considered to be related to Wrectariais the Neotropical Sipaneeae (Table l), which is no longer considered closely related to the Rondeletieae (Rova, 1999). Verdcourt (1953, 1958) previously mentioned the morphological similarities between Erectaria and Sipama. The two genera resemble each other in their herbaceous growth habit, indumentum characteristics, simple stipules, inflorescence structure and bilocular ovary. Sipanea differs mainly from Erectaria in the contorted aestivation, the oblong fruits and the exotesta. The prismatic seeds of Sipanea have isodiametric exotestal cells with verrucate thickenings along the inner tangential and radial walls and relatively large pores in the inner tangential walls. There are prominent thickenings in the angles of the exotesta cells, similar to those found in Wrectaria species. However, a close affinity between Wrectaria and Sipanea is unlikely. The morphological isolated position of Virectariawas probably best reflected by Verdcourt’s monogeneric tribe Virectarieae (Verdcourt, 1975). Since molecular evidence, however, is strong for the inclusion of Erectaria in the tribe Sabiceeae, we think it best t o consider it as an isolated genus within this tribe. zyxwvut zyxwvut Morphological and molecular evidence give conclusive reasons for excluding the genus Virectaria from the subfamily Rubioideae. Absence of raphides, strongly elongated and verrucate thickened exotesta cells, and stipule morphology support a position in the vicinity of the Sabiceeae sensu Bremer (subfamily Ixoroideae). A close relationship, however, with Sabicea, Pseudosabicea or Tamridaea is unlikely due to the high degree of unique features met in Erectaria. Erectaria is best considered as an independent evolutionary line within the tribe Sabiceeae. More intensive sampling and the use of more informative molecular and morphological data will possibly give us a better understanding of the phylogeny of these alliances. ACKNOWLEDGEMENTS We are grateful to Mrs D. M. Bridson for her comments on the manuscript. Technical support by Anja Vandeperre and Marcel Verhaegen is gratefully acknowledged. This study was supported by the Fund for Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 CONCLUSION zyxw zy zyxw SURVEY OF WRECTARIA Scientific Research-Flanders (F.W.O.) (project numbers 2.0038.91) and by a grant form the Research Council of the K.U.Leuven (OT/97/23). Suzy Huysmans is a postdoctoral fellow, and Steven Dessein a research assistant of the F.W.O. 23 Don G. 1834. General history o f the dichlamedeus plants. Vol. 3. London. Farris JS. 1983. The logical basis of phylogenetic analyses. In: Platnick N, Funk V, eds. Advances in Cladistics, Vol. 2. New York: Columbia University Press, 7-36. Hall JB. 1972. A new species of Erectaria (Rubiaceae) from Ghana. Kew Bulletin 26. 567-571. Halle N. 1966. Famille des Ruhiacees (Ire partie). Flow d u Gabon 12. Paris: Museum National d'Histoire Naturelle. Hiern WP. 1877. Order LXX. Rubiaceae. In: Oliver D, ed. Flora of tmpical Africa. Vol. 3. London: Reeve, 48. Hutchinson J, Dalziel JM. 1963. Rubiaceae. In: Hepper FN, ed. Flora of West Tropical Africa, ed. 2. London: Crown agents for oversea governments and administrations, 110111. Hooker JD. 1873. Ordo LXXXIV. Rubiaceae. In: Bentham G, Hooker JD, eds. Genera plantarum ad exemplaria imprimis in herbariis kewensibus servata defirmata. London, 7-151. Huysmans S, Robbrecht E, Smets E. 1993. Endoaperture morphology in the Coptosapelteae (Rubiaceae-Cinchonoideae). Kurzfassungen 11. Symposium Morphologie, Anatomie und Systematik, Salzburg, 66. Huysmans S, Robbrecht E, Smets E. 1998. A collapsed tribe revisited: pollen morphology of the Isertieae (Cinchonoideae-Rubiaceae). Review of Palaeohotany and Palynology 104: 85-113. IAWA Committee. 1989. IAWA list of microscopic features for hardwood identification. International Association of W i d Anatomists Bulletin n.s. 10: 219-332. Jansen S, Kitin P, De Pauw H, Idris M, Beeckman H, Smets E. 1998. Preparation of wood specimens for transmitted light microscopy and scanning electron microscopy. Belgzan Journal of Botany 131: 4 1 4 9 . Kiehn M. 1995. Chromosome survey of the Rubiaceae. Annals of the Missouri Botanical Garden 82: 398-408. Puff C, Igersheim A. 1994. The character states of Mussaendopsis Baill. (Rubiaceae-Coptosapelteae). Flora 189: 161-178. Punt W, Blackmore S, Nilsson S, Le Thomas A. 1994. Glossary of pollen and spore terminology. Utrecht: LPP Foundation. Reitsma T. 1969. Size modification of recent pollen grains under different treatments. Review of Palaeobotany and Palynology 6 9 23-47. Robbrecht E. 1988. Tropical woody Rubiaceae. Opera Botanica B e b c a 1: 10-271. Robbrecht E. 1994. Supplement to the 1988 outline of the classification of the Rubiaceae. Index to genera. Opera Botanica Belgmz 6 173-196. Rova J. 1999. The Condamineeae Rondeletieae Sipaneeae complex (Rubiaceae). D. Phil. Thesis, Goteborg University. Schumann K. 1891. Rubiaceae. In: Engler A, Prantl K, eds. Die naturlichen Pflanzenfamilien. Leipzig: Engelmann, 29-30. Schumann K. 1896. Rubiaceae Africanae. In: Engler A, ed. Botanische Jahrbucher fur Systematik, Pflanzengeschichte und Pfinzengeographie. Leipzig: Engelmann, 422. zyxw zyxwvutsr REFERENCES Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Andersson LA.1996. Circumscription of the tribe Isertieae (Rubiaceae). Opera Botanica Belgica 7: 139-164. Baerts M, Lehmann J . 1989. Guerisseurs et plantes medicinales de la region des cr6tes Zaii-e-Nil au Burundi. Annales Sciences Economiques 18: 214. Baerts M, Lehmann J. 1991. Plantes medicinales veterinaires de la region des cretes Zai're-Nil au Burundi. Annales Sciences Economiques 21: 133. Baillon H. 1880. Histoire des plantes. Paris: Hachette. Barthlott W, Elder N. 1977. Raster-Elekronenmikroskopie der Epidermis-Oberflachen von Spermatophyten. Tropische and Subtmpische Pflanzenwelt 19: 1-105. Bremekamp CEB. 1952.The African species of Oldenlandia L. sensu Hiern et K. Schumann. Verhandelingen der Koninklijke Netkrlandse Akademie wan Wetenschuppen, Afd. Nut., ser. 2, 48: 1-297. Bremekamp CEB. 1966. Remarks on the position, the delimitation and the subdivision of the Rubiaceae. Acta Botanica Neerlandica 1 5 1-33. Bremer B. 1987. The sister group of the paleotropical tribe Argostemmateae: a redefined neotropical tribe Hamelieae (Rubiaceae, Rubioideae). Cladistics 3: 35-51. Bremer B. 1996. Phylogenetic studies within Rubiaceae and relationships to other families based on molecular data. Opera Botanica Belgica 7: 33-50. Bremer B, Thulin M. 1998. Collapse of Isertieae, re-establishmenl, of Mussaendeae, and a new genus of Sabiceeae (Rubiaceae);phylogenetic relationships based on rbcL data. Plant Systematics and Evolution 211: 71-92. Bremer K. 1994. 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APPENDIX 1 SPECIMENS FROM BR & WAG USED FOR DISTRIBUTION MAPS Erectaria angustifolia (Hiern) Bremek. CAMEROON: NE 0210: 15km SSE de Zingui, Letouzey 9011 (BR810137) - NE 0508: Ndian river, West of Mundemba, Nem ba & Thomas 321 (BR 807327); Barrage de Kinguele, de Wilde, Arends, de Bruijn (WAG) - NE 0509: Between Abat and Bayib Ossing, 20km WNW Nguti, Letouzey 13809 (BR 807324). GABON: NE 0010: Mfoa, tributary of Nkomo river, 85 miles E of Gaboon, Bates 528 (BR810170) - SE 0210: Chantier CEB, 35 km SW of Doussala, Reitsma, Breteler &Louis 1063 (WAG). Vrectaria angustifolia (Hiern) Bremek. var. schlechteri Verdc. CAMEROON: NE 0409: Inter Mafura e t Mundame, Schlechter 12926 (BR810143). Vtrectaria beZingana N.Halle GABON: NE 0010: Rocher de Abanga, top of the rock, Bos, uan der Laan & Nzabi 10624 (BR807360) - NE 0011: Inselberg c. 28 km ESE of Medouneu, Reitsma & Louis 1793 (WAG) - NE 0113: Road on Babiel-Nord, few km W of Belinga, Bos, van der Luun & Nzabi 10692 (BR 810176). CAMEROON NE 0211: Akoakas Rock, 24km on the road from NKoemvone to Ambam, de Wilde 7693 (BR 901680). Vtrectaria herbacoursi N.Halle GABON: NE 0011: Inselberg, c. 28 km ESE of Medouneu, Reitsma & Louis 1816 (WAG) - SE 0111: 45km along the road from Mbigou to Lhbamba, de Wilde, Arends, Louis, Bouman & Karper 560 (BR808005). Vtrectaria major (K.Schum.) Verdc. subsp. major BURUNDI: SE 0229: Cibitoke, Reekmans 358 (BR837235) - SE 0230: Kanzigiri, Kitete lac, Elskens 53 (BR809939) - SE 0329 Bubanza, Musigati, Lewalle 419 (BR 809927); Bugarama, Bouharmont 11163 (BR 901511); Bujumbura-Missumba, Lewalle 643 (BR 809924); Bujumbura, Nyabiraba, Reekmans 686 (BR?); Bujumbura-Kanyosha, Lewalle 5084 (BR810036); Bururi, Bequet 164 (BR 901410); BweruKaruzi, Van der Ben 1987 (BR810048); Entre Isare et Muramvya, Robyns 2291 (BR 901409); Gakara, mine de bastnesite, LewaZle 3579 (BR 810155); Honga, Lewalle 6206 (BR810066); Karuzi-Muhinga, Van der Ben 1772 (BR 810081); Kisozi, Germain 8857 (BR 810033); Kisozi, Lejeune 131 (BR 901402); Muramvya, Bugarama, LewalZe 4601 (BR901516); Muramvya, Bugarama, Lewalle 5365 (BR 809997); Muramvya, Mont Teza, Nyabigondo, LewaZZe 6683 (BR 901518); Muramvya, Nyabigondo, LewalZe 1613(BR 901515); Muramvya: Teza (Catare) talus bord chemin forestier, Reekmans 10916 (BR 901519); Muramvya, Teza, Reekmans 2367 (BR 809931); Parc Kibira, zone Rwegura, Breyne 6037 (BR901514); Pres de Muramvya, Symoens 2333 (BR 810180); route GitegaBujumbura km 62, Muramvya, Baudet 313 (BR 901550); Bouharmont 22332 Ruibaga, Mugongomanga, (BR 901513); Source du Nil-Bututsi, Michel 4685 (BR 901415); Ruibaga, Mugongomanga, Bouharmont 22344 (BR 901512); Teza, Reekmans 6649 (BR 901520) - SE 0330: Karuzi, MicheZ4919 (BR901517); Rusengo, Buyogoma, Michel 4008 (BR 809994); Rusengo, Buyogoma, Michel 4284 (BR 810163); Vallee Ruvubu, territoire Ruyigi, Reekmans 3089 (BR807388) - SE 0429: Gahama, S du Bugesera, Liben 1174 (BR809945). CAMEROON: NE 0409: Manengouba Mts. base, 4 km WNW of Nkongsamba, Leeuwenbelg 8288 (BR 810186); Manengouba Mts. WNW of Nkongsamba, Leeuwenbelg 8841 (BR 810059); Piste de Bangem, aux lacs du Mangouba, 15km NW Nkongsamba, Letouzey 14388 (BR810069) - NE 0411: Mont Golep, 36km au N de Bafia, Letouzey 9586 (BR810051); Mont Yangba pr6s de Nyafianga (42 km NNE de Bafia), Letouzey 7817 (BR) NE 0509: Pinyin, SonkB 415 (BR810094) - NE 0510: Col de Bana (15 km E Bafang), Letouzey 13301(BR 810160); Near Dschang, PauZy 331 (BR837232); Mbouda, C.N.A.D. 1469 (WAG); Djuttitsa, Dschang 137 (WAG) NE 0610: Jakiri, Hepper 2067 (BR808007) - NE 0611: Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Smith JE.1817.Vzrecta. In: Rees A, ed. The Cyclopedia, or universal dictionary of arts, sciences and literature, vol. XXXVII, 2. Stearn WT. 1966.Botanical Latin. London: Nelson, 506-507. Swofford DL. 1999. Paup*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland Sinauer Associates. Van Steenis CGGJ. 1981. Rheophytes of the world. Alphen a/d Rhijn: Sijthoff & Noordhoff. Verdcourt B. 1953. A revision of certain African genera of herbaceous Rubiaceae. I11 The genus Vzrectaria Brem. Bulletin du Jardin Botanique de l’Etat 23: 35-52. Verdcourt B. 1958. Remarks on the classification of the Rubiaceae. Bulletin du Jardin Botanique de l’Etat 28: 209-28 1. Verdcourt B. 1975.New sectional name in Spermacoce and a new tribe Virectarieae. Kew Bulletin 30:366. Verdcourt B. 1993. Rubiacees nouvelles pour la Flora Zambesiaca. Bulletin du Jardin Botanique National de Belgzque 62:415417. Weberling F.1977.Beitrage zu Morphologie der RubiaceenInfloreszenzen. Berichte der Deutschen Botanischen Gesellschaft 90:191-209. White F.1978.The afromontaneregion. In: Werger M A , ed. Biogeography and ecology of southern Africa. The Hague: Junk, 463-513. White F. 1979. The Guineo-Congolian Region and its relationships to other phytochoria. Bulletin du Jardin Botunique National de Belgzque 4 9 11-55. White F. 1993. The AE’ITAT chorological classification of Africa: history, methods, and application. Bulletin du Jardin Botanique National de Belgzque 6 2 225-281. Wilkinson HP. 1979. The plant surface (mainly leaf). In: Metcalfe CR, Chalk L, eds. Anatomy of the Dicotyledons, Vol. 1. Oxford: Clarendon Press, 97-165. zyx zy z zyxwvu zyxwvut zyxwv SURVEY OF VIRECTARIA Biano, Homble 893 (BR809412) - SE 0927: A 13km au NNE de Sampwe, Lisowski, Malaisse & Symoens 11060 (BR901753) - SE 1027: A env. l l k m a 1'WNW de la source occidentale de la Lutshipuka, Lisowski, Malaisse & Symoens 3879 (BR901691) - SE 1127: Entre Bugwe et Kalwe, Hendrickx 199b (BR809933). RWANDA: SE 0129: Km 12 route Gitarama-Ruhengeri, Troupin 14424 (BR 901508); N Rwanda, Bulera meer, N oever, Van der Veken 9390 (BR807325) - SE 0130: Mohasi, Mildbraed 460 (BR809993) - SE 0228: Territoire de Shangugu, Michel 5096 (BR901449) - SE 0229: 5 km avant Gisakura (venant de la route ButareCyangugu), Van der &ken 11095 (BR807325); Au km 31 de la route Butare-Cyangugu, Auquier 2771 (BR 901458); Bunyambilili-Lange, Neel41 (BR 901445); Butare, Bouxin 1455 (BR 901606); Colline Kalongi, commune Gitesi, km 10 des bureaux de la prefecture de Kibuye, Nuyt 167 (BR 901444); Colline Kanzi, commune Nyaruhengeri, Bouxin & Radoux 1831(BR901453); Colline Nyabisindu. Commune Nshili, Nuyt 239 (BR901443); Forgt de Nyungwe environ de Rwankuba, Bouxin 383 (BR 901607); Foret de Nyungwe, environs de Mayembe, Bouxin 63 (BR901456); For& de Rugege (Cyangugu), au km 109 de la route Butare-Cyangugu, Auquier 3363 (BR 901457); Foret de Nyungwe, colline Rukuzi, Bouxin 608 (BR901455); For6t de Nyungwe, environs de Mayebe, Bouxin 881 (BR 901452); For6t de Nyungwe, route Butare-Cyangugu, km 110, Bouxin & Radoux 613 (BR 901545); Gisovu, station forestiere Suisse, Troupin 14612 (BR901510); Ihembe, km 117 de la route Butare-Shangugu, Reynders 88 (BR 901500); Kitabi, 51 km route Butare-Cyangugu, Bridson 147 (BR901451); km 12 route Gitarama-Kibuye, a hauteur du pont sur la riv. Nyabarondo, Troupin 14495 (BR 901509); km 40 route Usa-Butare, Hendrickx 7430 (BR 901620); Mt Tshikungu (Idjwi), Hendrickx & Germain 6731 (BR 901605); Route Butare-Bukavu, vers km 104, environ dUwinka, Troupin 11502 (BR901503); Route Butare-Bukavu, vers km 93, environ Shangugu, dUwinka, colline Buynangurube, Troupin 11942 (BR 901505); Route Butare-Bukavu, vers km 93, environ dUwinka, colline Wakagano, Troupin 11232 (BR901502); Route Butare-Bukavu, vers km 93, riviere Banda, Troupin 11852 (BR 901504); Route Bukavu-Butare, marais Kamiranzovu, Troupin 12285 (BR 901506); Route Bukavu-Butare, vers km 98, environ dUwinka, Troupin 13034 (BR 901507); Route Gitarama-Ruhengeri, 13km de Gitarama, Bouxin & Radoux 2136 (BR 901459); Rubona-Ineac, Michel 5315 (BR901450); Rubona-Ineac, Michel5757 (BR 901448); Rubona-Ineac, Michel 6235 (BR 901447); Rubona-Ineac, Michel 6323 (BR901446); Rutovu vers km 62 de la route ButareShangugu, Reynders 294 (BR901501) - SE 1034: Shangugu, route Bukavu-Butare, environ de Nyungwe, Troupin 10367 (BR808010); Shangugu, route BukavuButare, envion d'Uwinka, Tmupin 9698 (BR808013) SE 1127: Kalyabirondo, Kalwe, Hendrickx 554bis (BR 809936). TANZANIA: SE 0131: near Bukoba, Haarer 2138 (BR810159) - SE 0230: Kirushya, Bugufi, Ngara, West Lake Province, Tanner 4826 (BR810085) - SE 0429: Kalinzi, Buha district, Verdcourt 3399 (BR 810071) SE 0430: Selimweguru, Kungwe Mountain, Western province, Kigoma district, Newbould & Harley 4602 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 Petit Yoli prks Mayo Darle (40 km SO Banyo), Letouzey 8690 (BR 810084). CONGO: NE 0029: Entre Beni et Lubero, Lebrun 4242 (BR 807322); le long de la piste Kalonge-Mutwanga, de Witte 8134 (BR809943); Nord-Kivu, 29km au S de Butembo, Lisowski 17793 (BR 901658); Nord-Kivu, 29 km au S de Butembo, Lisowski 17793 (BR901522); Ruwenzori (Butange), Bequaert 3584 (BR 901439) - NE 0128: Haut-Za'ire, Ituri, env. de Nduye, Mont Makikbo, Lisowski 44716 (BR 901532) - SE 0029: Bwito, Kihondo, Colline Kikuku, Deru 152 (BR 809932); Hintumo pres Musavoki (reg. Tshiaberimu), de Witte9992 (BR 809946); Kasisi (Tshiaberimu), de Witte 12202 (BR 901557); Musimba (pres Musavoki) reg. Tshiaberimu, de Witte 9935 (BR 809926); Musimba reg. Tshiaberimu, de Witte 12172 (BR809929); reg. Tshiaberimu, de Witte 9973 (BR 809949); Secteur Kisaka, Mont Bukara, Heine 269 (BR809938) - SE 0129: Environ de Migeri, de Witte 8759 (BR 901608); Kabango, Bequart 6137 (BR 901408); Kaitafu, Bequaert 6036 (BR 901406); Kamatembe, de Witte 1563 (BR 901440); Munagana, de Witte 1883(BR?) - SE 0228: Brousse de Tshamussi, Scaetta 628 (BR 809937); Bugwe, Kalya-Birondo, Hendrickx 199a (BR 901441); Bugwe, Kalya-Birondo, Hendrickx 299 (BR 901442); Bukavu-Kisangani km 32, Breyne 1738 (BR 810063); Bukulumisa, Hendrickx 1504 (BR 809940); Bushanganya, Hendrickx 5802 (BR 809928); Colline Nakaziba, Territ. Kabare (Kivu), Vermylen 99 (BR 809935); Ile-shime, Hendrickx 5036 (BR 810017); Ineac-Nyamunyunye, Pierlot 444 (BR 810102); Kahuzi, Meurillon 951 (BR 901525); Kalama, Van den Houdt 219 (BR901405); Kalehe, Sintama, Van der Ben 143 (BR?); Katan, Kivu, Lushasha, De Wulf 36 (BR901399); Kimanyaho-Nzibira, km 79 Bukavu-Shabunda. territoire de Kabare, Pierlot 2564 (BR901526); Kivu, Mont Kahuzi, pres du Poste Mukaba, Lisowski 10585 (BR901523); Marais de la Musisi, km 23 Kavumu-Walikale, Pierlot 2042 (BR 810114); Mont Kahuzi, terr. Kalehe, Ntakiyimana 18 (BR 901610); Montagnes a l'ouest du Lac Kivu monts Biega, Humbert 7574 (BR 901407); Mt. Bukulumiza Ineac-Mulungu, Pierlot 297 (BR 810168); Mulungu, Ghesquiere 6449 (BR901404); Ngondjola a Ludaha, Laurent 302 (BR810089); Route Bukavu-Walikale, a droite de la route, Petit 25 (BR 901624); Route Bukavu-Walikale,km 40, Petit 21 (BR901524); Route Bukavu-Walikale km 48, Petit 256 (BR 901527); Route Bukavu-Walikale Ten: Kabare, Leonard 1445 (BR 901521); Tshibinda Bukulumiza, Pierlot 60 (BR 810135); Walungu, Kaleare, Laurent 627 (BR810116) - SE 0229: Ile Idjwi dans le lac Kivu, Humbert 8349 bis (BR901403) - SE 0727: Manono, Katanga, Marlier 1696(BR901533) - SE 0727: Mashi: Munuwindama a Kaziba, Laurent 570 (BR810092) - SE 0729: Haut-Shaba, Domaine de Muhila, pres de Kinianta, Mont Kiseye, Lisowski 60293 (BR901539) -- SE 0729: Lusinga (Plateau des Kibra, Katanga), Lisowski, Malaisse & Symoens 5080 (BR901435) - SE 0827: Au N. de Mitwaba, Symoens 3561 (BR 901 460); Kalumengongo, ck Witte 05952 (BR810185); Kibara, de Witte 06090 (BR901616); Kibara, riv. Manda, de Witte 06034 (BR901621); Mukana, de Witte 02423 (BR901556); Plateau des Kibara, Lisowski, Malaisse, Symoens 4394 (BR 837229) - SE 0925: Plateau de Biano, Hom bl6 853 (BR 809954); Plateau de 25 zyxwvu 26 zyxwvutsrq zyxwvutsrq zyxwvutsrq S. DESSEIN ET AL. z zyxw zyxwvuts zyxw Virectaria major (K.Schum.) Verdc. subsp. spathulata (Verdc.) Dessein & Fbbbr. CAMEROON: NE 0210: Nkolebenga, colline au NO d'Ebianemeyong, pres Nyabessan (60km E de Campo), Letouzey 10357 (BR901544) - NE 0211: Rocher Ako'okas, 24km on the track leading from NKoemvone SE to Ambam, de Wilde 7460 (BR810060) - NE 0409: Piste Manengouba-Mt. Manengouba, Bamps 1551 (BR 901552). CENTRAL AFRICAN REPUBLIC: NE 0520: Bimbala, 80 km E Bambari, Tisserant 2284 (BR901710). CONGO: NE 0018: Basankusu, Lulongo, Dubois 482 (BR 901438); Bombimba, Ikelemba, Laurent 1186 (BR 901496); Coquilhatville, Pynaert 286 (BR 809952); Coquilhatville, Schlechter 12599 (BR 810132); Eala, Laurent 1605 (BR901495); Eala, Lebrun 1193 (BR 808002); Eala, Pynaert 1692 (BR 901425); Eala, Staner 1559 (BR810104); Ikelemba, Bmun s.n. (BR810138); Mampoko, Bruneel s.n. (BR901728) - NE 0022: Djolu, riv. Bolombo, Eurard 5761 (BR810141) NE 0024: A 22km a 1'Est de Yangambi, Louis 16099 (BR 809948)*; Busukuru, Louis 7874 (BR 901651)*;Yangambi, a l'embouchure de la riviere Litirumbu, Louis 7956 (BR 809925)*; Yangambi, ile Esali, Louis 10971 (BR 807355); Yangambi, km 6 route de Ngazi, Louis 561 (BR 901632); Yalulia, a 20 km a l'E de Yangambi, Louis 9599 (BR 808004); Yangambi, Louis 13758 (BR901417); Yangambi, Ple Baleke, Louis 11575(BR 901419);Yangole, a 25 km au NW de Yangambi, Louis 12153 (BR901416) - NE 0025: 60km au N de Kisangani, Bengamisa, Liswoski 15269 (BR901499) - NE 0119: Basankusu, Bruneel s.n. (BR901695); Makanza, De Giorgi 312 (BR 901422); Makanza, De Giorgi 251 (BR 901434); Nouvelle Anvers, De Giolgi 1174 (BR901414); Songo, terr. Befale, Eurarcl 3330 (BR810105) - NE 0125: Banalia, Bequaert 1379 (BR 901497); Haut-Zdire, Banalia, 1km a 1'W de l'Aruwimi, Lisowski 47518 (BR901535) - NE 0128: Epulu and vicinity, about 200 miles east of Stanleyville, Putman 69 (BR 901426) - NE 0220: Likimi, De Giorgi 1590 (BR901421) - NE 0221: Boyango St Paul, Robyns 1067 (BR810029)* - NE 0223: Mobwasa, Reygaert 1178 (BR901424) - NE 0224: Buta-Bima, Seret 61 (BR 810165) - NE 0227: Nala, Boone 192 (BR 809934)* 0320: Boyasegeze (Bongo), Eurard 1503 (BR901411) - NE 0425: Tukpwo, Gerard 4256 (BR901547); Tukpwo, G'erarcl 4139 (BR901612) - SE 0018: Ikenge, Huyge s.n. (BR901629) - SE 0022: Mondombe, Jespersen 186 (BR810147) - SE 0024: Opala, Louis 14210 (BR901413);Yaolika, entre Yaluwe et Ekoli, s u r le Lomami, Louis 13376 (BR 901420); Yapehe (Bambole), rive gauche en face de Yangambi, Louis 11221 (BR901418) - SE 0025: Au Sud de Pene-Tungu, Lejoly 2934 (BR 901540) - Haut-ZaYre, 20 km a l'Est dUbundu, Lisowski 48120 (BR901614) - SE 0123: Ikela, Eurard 5566 (BR810174); Ikela, Germain 7401 (BR810108) SE 0128: Route Kavumu-Walikale, vers km 110, environ d'Irangi, Troupin 12090 (BR901554); Route KavumuWalikale, vers k m 110, Irangi, reserve Irsac, Troupin 6421 (BR901555); Vers km 10 route Kavumu-Walikale, Irangi, reserve Irsac, Troupin 6414 (BR 901553); Kalehe, route Kavumu-Walikale, vers km 111, Troupin 3397 (BR 901747); Kalehe, route Kavumu-Walikale, vers km 110, Irangi, reserve 1.R.SA.C. Catena I, Troupin 10760 (BR901534); Route Kavumu-Walikale, vers km 110, Kalehe, Troupin 10126 (BR 901623); Route Kavumu-Walikale, Kalehe, Troupin 10154 (BR901541) - SE 0316: Gambony, Vanderyst 3672 (BR 901428) - SE 0317: Bandundu, Vanderyst 5137 (BR 901430); Dima, Vanderyst 5103 (BR837228) - SE 0415: Kinshasa, Bouhurmont 7208 (BR 837251) Kinshasa, Bequczert 7530 (BR 810171); Stanley-pool, entre Leo et Sabuka, Duchesne 39 (BR 901429); Kimuenza, Gillet 1789 (BR 901733); Kibuanga, terr. Kimbanseke, Pauwels 5879 (BR 901615); Luebo-Kasai, Achten 95b (BR809951) - SE 0426: Kasongo, Clczessens 551 (BR810000) - SE 0513: Baya, Kwilu, Vanderyst 2621 (BR901401) - SE 0515: Kisantu, Gentil556 (BR901665); Kisantu, Gillet s.n. (BR901545) - SE 0619: Kisanji, Renier 60a (BR 901400) - SE 0718: chutes de la Kwenge a Bwana, Mutombe, Callens 3156 (BR901529). IVORY COAST: NW 0708: Mont Momi, pres de Danuane, Hall6 389 (BR810074). SIERRA LEONE: NW 0811: Jigaya, Thomas 2534 (BR 807363). - NE Virectaria multiflora (Sm.) Bremek. CAMEROON: NE 0212: Rocher dAkoafim, 38 km SSE de Djoum, Letouzey 8356 (BR901650) - NE 0311: NW of village Nkolbisson, 7 km W of Yaounde, Breteler 1920 (BR901690) - NE 0614: Mbalarzi, dans la vallee de la Mbere (65km a vol doiseau au NE de Meiganga), Letouzey 6194 (BR901622). CONGO: NE 0018: Eala, Laurent 1196 (BR901676); Eala, Pynaert 1153(BR 901643); Eala, route de Bolombo, Robyns 615 (BR901655); Eala, Vermoesen 2131 (BR 901721); Coquilhatville, Goossen 3089 (BR 901732); Eala, Eurard 3090 (BR901672); Eala, Corbisier 1111 (BR901705); Eala, Leemans 427 (BR 901671); Eala, Staner 1335 (BR 901688); Chemin Bantoi-Eala, Couteaux 2 (BR901656) - Jachere Eala, Couteaux 264 (BR 901675); Eala, Lebrun 264 (BR 901668); Eala, Claessens 14 (BR901757); Eala, Louis 213 (BR809944); Eala, Staner 1415(BR 901681); Sentier vers Wangata-Watsiko (env. dEala), Leonard 211 (BR808014) - NE 0119: Makanza, de Giorgi 17 (BR901699); Makanza, de Giorgi 381 (BR901666) - NE 0123 Barumbu, Claessens 36 (BR901724) - NE 0227: Makeke, Curlier 337 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 (BR810052) - SE 0630: Mpanda District: KungweMahali Peninsula, Harley & Newbould 4646 (BR 810129)- SE 0835: Iringa, Mufindi, G'e~au& h u e t t 3009 (BR810015) - SE 0935: Stromgebiet des oberen Ruhudje, Landschaft Lupembe, Schlieben 296 (BR810005). UGANDA SE 0030: Igara, Ankole, Pursegloue 573 (BR810006) - NE 0031: Lake Buwyoni, Kigezi District, Rogers, Gardner 274 (BR901678) - NE 0232: Mushungero, lake Mutunda, Chandler-Hancock 2608 (BR810073) - SE 0029: R. Nyamugasani valley, Osmastan 2151 (BR810027) - SE 0031: Kigezi district, Paul0 676 (BR 810072); Kigezi District, Rogers & G a d ner 352 (BR 810039) - SE 0129: Kigezi Dist., Bufumbira, Mushungyero, Katende 158 (BR810096). ZAMBIA: SE 0831: Abercorn, Bullock 2171 (BR810099); Ndundu, drive Mbala, Sanune 943 (BR810050); Ndundu, Richards 21458 (BR807393) - SE 1231: Riverine forest above Ballymain, Banks of Minambo Stream, Richards 1716 (BR810026). zyxwvutsrqp zyxwv zyxw zyxwvutsrq zy SURVEY OF WRECTARIA cassava garden, Bos 2288 (BR810134) - Paynesville, Bouhurmont 12144 (BR 901685) - Paynesville, 8 miles E of Monrovia, Voorhoeue 100 (BR901684) - NW 0709: 3 miles NE of Suacoco, Gbarnga, Central Province, Daniel 27 (BR 901652): 3 miles NE of Suacoco, Gbarnga, Central Province, Daniel 110 (BR 901731); Loffa county, Gbarnga-Zorzor road, along small tributary to the St. Paul river, Bos 2506 (BR 901648); Zorzor-Gbarnga road, W of St. Paul river, Bos 2161 (BR901723). NIGERIA: NE 0508: Oban, group F.R. in an old farmland, Daramola 56397 (BR901548). R.C.A.: NE 0318: Rkgion de Mbalki e t Boukoko, nsserant 1896 (BR901644). SENEGAL,: NW 1216: Basse-Casamance, Mpak, Vanden Berghen 1899 (BR 810131); Basse-Casamance, Bouyouyow, Vanden Berghen 2553 (BR 810002); Basse-Casamance, Bofa Bayot, Vanden Berghen 3958 (BR 810065); Basse-Casamance entre Brin et Essil, Vanden Berghen 5447 (BR810032); Chemin de Brin vers Essil, environ de Badiat-Grand, Champluvier S109 (BR 810042) - Tobor, Vanden Berghen 1310(BR 810164); Toubakouta au S de Ziguinchor, Vanden Belghen 2120 (BR 810098). SIERRA LEONE: NW 08011: Njala (Kori), Pyne 2 (BR 810162). Wrectaria pmcum bens (Sm.) Bremek. CAMEROON: NE 0209: 7 km from Kribi, 2 km N of Ebolowa road, Bos 5325 (BR 837246) - NE 0211: Station du Cacaoyer de N’Koemvone 14 km on the road from Ebolowa to Ambam, de Wilde 7571 (BR808017); Station du Cacaoyer de N’Koemvone, about 14 km on the road from Ebolowa to Ambam, de Wilde 7757 (BR808016) NE 0214: A 28km a I’ENE #ETA, soit a 52km au SE de Ngoila (Axe Lomie-Souanke), Letouzey 11973 (BR901746) - NE 0310: Bipinde, Zenker s.n. (BR901713) - NE 0312: Ruisseau Sougwa a 15km au S de Djouo (20 km E de Domaloma sur de DJA), Letouzey 4431 (BR901649) - NE 0313: 3 km N of Lomie, Leeuwenbelg 6516 (BR901748) - NE 0315: A 25 km au NE de Bange (km 75 route Yokadouma-Moloundou), Letouzey 5120 (BR901715) - NE 0409: E side base Mt. Nlonako, between Enyunguengue Ngalmoa and Quartier Ekanmbeng, 10 km SE of Nkongsamba, Leeuwenberg 8391 (BR901744) - NE 0414: A 27km au SSW de Koso (village situe a 60km au SSW de Batouri), Letouzey 5512 (BR901646). NE 0508: Path from Fabe-Mundemba road to Makeke Camp, Manning 94 (BR901711) - NE 0509: Cascade (10 m) de la riviere Akoumayip sur piste d’Agborkem a Tabo, 20km W Mamfe, Letouzey 13738 (BR 901679). CONGO: Kikixit, Vanderyst 9066 (BR901696) - NE 0024: Yangambi, Leonard 81 (BR 901703); Yangambi, Louis 15977 (BR901640); Yangambi, km 15 route de Ngazi direction W, Louis 547 (BR901631); A 25 km a 1W de Yangambi, Louis 3423 (BR809941); A 11km a 1’E de Yangambi, Louis 3141 (BR807342); Yangambi, Louis 9796 (BR809950); Yangambi, le long de la riviere Isalowe, Louis 9805 (BR809955); A 15km au NE de Yambao, vallee marecageuse de la Lombo, Louis 15888 (BR901669) - NE 0025: Kisangani, zone de Kabende, localite Kibidi, Lisowski 52541 (BR837226); 22 km au N de Kisangani pres de Bawombi, Lisowski 47842 (BR837244); route Kisangani-Opala, 25 km au S de Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 (BR901736) - SE 0017: Gombe, Sapin s.n. (BR901741); Gombe (equateur) Sapin s.n. (BR901635) - SE 0218: Kutu, Laurent s.n. (BR901700) - SE 0317: Bandundu, Vanderyst 5168 (BR901657); Bokala, Nelis s.n. (BR 901633); Kwango, Vanderyst s.n. (BR 901667); Wombali, Vanderyst 1952 (BR 901692); Wombali, Vunderyst 1839 (BR 901758); Wombali, Vanderyst 2326 (BR 901725); Wombali, Vanderyst 758 (BR 901701); Wombali, Vanderyst 1284 (BR901734) - SE 0411: Kouilou, 44km au N de Pointe Noir, 2 k m au N de Tchissanga, Lisowski B-7189 (BR901551) - SE 0415: Kimuenza, vallee de la Kalamu, Eurard 6401 (BR901546); Kimuenza, Gillet s.n. (BR 901634); Kinshasa, Achten 137 (BR 901611); Kinshasa, Bequaert 7323 (BR 901642); Kinshasa, Coateaux 1054 (BR 901639); Kinshasa,Jans 61 (BR 901738); Lovanium, Breyne 454 (BR 901709); Ludjumba, Dolo, Bavicchi 435 (BR901609); Maluku, au dela de la Nsele, Pauwels 4872 (BR901742); Marais du Stanley pool, Hens 64 (BR 901659); Ndjili, derriere la plaine, Kinshasa (Kisantu), Pauwels 4717 (BR901543); Stanley Pool, Kinshasa, Eurard 6 (BR 901722); Stanley-Pool, Schlechter 12553 (BR901704) - SE 0513: Bingila, Dupuis s.n. (BR901743); Bingila, Dupuis s.n. (BR901754) - SE 0515: Kisantu, le long du chemin de fer, Callens 2047 (BR901687); Kisantu, Gillet 890 (BR 901755). CONGO (BRAZ): SE 0014: Parc National dOdzala, Champluvier 5092 (BR 901647). EQUATORIAL GUINEA: NE 0109: Bata-Borne, Caruulho 4987 (BR901677). GABON: SE 0009: Eastern part of the Presidential Reserve Wonga-Wongue, about 100km S of Libreville, de Wilde, Arends, Louis, Bouman & Karper 897 (BR901717) .- SE 0011: Near Achouka, Louis, Breteler & de Bruijn 570 (BR 837234) - SE 0111: Lebamba-Eteke, district de Mimongo, Halle & Cours 5864 (BR810110); Seka, 7 km along the road from Mimongo to Lebamba, de Wilde, Arends, Louis, Bouman & Karper 427 (BR901625)-- SE 0211: 25 km SSE of Doussala, de Wilde & Jongkind 9351 (BR 901461). GUINEA: NW 0809: Macenta-Gneckedou, Adam 5757 (BR 810169); pres de la ville de Macenta, Lisowski 60297 (BR810008) .- NW 1012: Friguiagbh, plantation de la Ouatamba, Chillou 656 (BR 901437); Friguiagbe, Chillou 3364 (BR810095) - NW 1014: Region de Boffa, pres de Tugnifily, Lisowski 51416 (BR901549) - NW 1215: Arredoi-es, Santo 2785 (BR810136). GUINEA BISSAU: NW 1115: Bissau, Bijimita, Santo 1770 (BR810047). IVORY COAST NW 0504: Near Brafouedi, 75km NW of Abidjan, Leeuwenberg2295 (BR810014); Small mountain c. 3 km E8of Becedi; c. 45 km NNE of Dabou, NW of Abidjan, de Wilde 672 (BR810103) - NW 0503: Near Grand Bassam, NW along road to Aboisso, Breteler 5979 (BR810167) .- NW 0604: 35km SW of Dimbokro, de Wilde 3219 (BR): Orumboboka, 40km S of Toumodi, Bokdum 2780 (BR809999) - NW 0608: Montagne de Kaodguezon, ‘Toulepleu,Guillaumet 1874 (BR810011) NW 0705: Baoule Nord, Chevalier 22319 (BR810044) NW 0708: Mount Nimba, Geerling & Bokdum 1699 (BR 810077). LIBERIA: NW 0510: Grand Bassa, Dinklage 1762 (BR901716) - NW 0610: Monrovia, Dinkluge 3240 (BR 901645); .Mount Coffee road, near Monrovia, native 27 zyxwvutsrq 28 zyxwvutsrq zyxwvut zyxwvutsrqp zyxwvut S. DESSEIN ET AL. zyx Kisangani, Lisowski 18379 (BR837238) - NE 0026: h a l i t e Banali, village Mengwe (km 88, route de PeneTungu a Lubutu), Lejoly 81/492 (BR 837243) - NE 0029: Parc National Albert, riviere Abyalose, Freakricq 9547 (BR837233) - NE 0124: Yambuya, Bequaert 1279 (BR901664) - NE 0128: Ituri, env. de Nduye, au NE de Maitatu, Lisowski 45122 (BR837241) - NE 0222: Dundusana, Mortehan 594 (BR 901729)- NE 0223: Mobwasa, Reygaert 457 (BR901674); Mobwasa, Reygmrt 887 (BR901628) - NE 0318: Entre Libenge et Zongo (Ubongi), Lebrun 1676 (BR901630) - NE 0320 Bodangabo, Evrard 983 (BR901636) - NE 0325: Angodia, Lebrun 2993 (BR901745); Bambesa, Gerard 4692 (BR 901536); Bambesa, Gerard 4692 (BR 901536); Bambesa, Gerard 5387 (BR 901637)- NE 0429: Parc National de la Garamba, R s t e centrale vers km 73 affluent de la Kasi, Tmupin 1713 (BR901538) - Nangaliwi, De Graer 805 (BR901663) - SE 0018: Ikengo, Lebrun 772 (BR901641) - SE 0024: Ekoli, s u r le Lomami, Louis 13365 (BR901673) - SE 0026: Parc National de la Ma’iko, 45km au Nord de Lubutu, Pene Aluta, rive droite de la Ma’iko, entre les affluents Ukungu et Utambe, Lejoly 1869b (BR 837242) - SE 0128: Kembe, Terr. Walikale, Leonard 1474 (BR 901739); Route KavumuWalikale, vers km 110, environ dIrangi, Catena 111, Troupin 9340 (BR901537) - SE 0411: Kouilou, Bena, Lisowski B-7130 (BR810152) - SE 0414: Lutete, Hens 321 (BR901702) - SE 0419: Ipamu, Vanderyst 12856 (BR 901730); Ipamu, Vanderyst 9893 (BR901706); Ipamu, Vanderyst 12751 (BR 901697) - SE 0514: Entre Zundu et Timansi, riviere Mpioka, Breyne 2512 (BR901708) - SE 0515: Kimvula terr. Popokabaka, Pauwels 290 (BR 901670); Kisantu, Gillet 3607 (BR901712). CONGO (BRAZ): SE 0411: km 50 Leubeme-PointeNoire, Breyne 5135 (BR 837227). GABON: NE 0009: Prov. Estuaire, Cap Esterias, along road south of plage de la Blondine, Andersson & Nilsson 2274 (BR837245); Prov. Estuaire: for6t de Mondah on road Librevill-Cap Esterias, Andersson & Nilsson 2288 (BR 837239). GHANA. NW 0600: Gbadzene nr.Amedzafe, Hull 40021 (WAG). GUINEA Friguiagbe, ChiZZou 898 (BR 901707). IVORY COAST NW 0407: about 3 miles south of Tai and just off road to Tabou, Boughey 14945 (BR 837240); about 3 miles south of Tai and just off road to Tabou, Boughey 14940 (BR 837230) - NW 0504: For& de Banco (Abidjan), Tehk 276 (BR 901660); Banco Forest Reserve, de Koning 6095 (WAG) - NW 0505: 9 km SW of KapotuAidou, Beentje 122 (WAG)- NW 0506: 43 k m E of Soubre, about 4km SE of Guedeyo, Leeuwenbelg 2172 (BR 809947) - NW 0708: Yeale, Geerling& Bokdam 1847 (BR 901693) - NW 0505: Along road from Dakpadou t o Sago, Geeding& Bokdam 2340 (BR 901726) - NW 0507: 17km N of Grabo, Breteler 7412 (BR901682) - NW 0707: Le long de la route du Mont Tonkoui WNW de Man, Cremers 1107 (BR809953) - NW 0708: Yeale, Geerling & Bokdam 1847 (WAG) - NW 0803: Near Yanse, Geerling & Bokdam 722 (WAG). LIBERIA: NW 0047: Eastern Province, Putu district, new road from Chiehn to Cape Palmas. Near Kanweake, a small village situated c. 70km S of Chiehn, de Wzlde & Voorhoeue 3696 (BR 901727) - NW 0508: 20 miles N of Sinoe, Jansen 1098 (BR809956) - NW 0608: Sia Town, Adam 16340 (BR901735) - NW 0708: Nimba Mts. Near Iron mine of L.A.M.C.O., Leeuwenbelg & Voorhoeve 4662 (BR901661) - NW 0709: 3 miles NE Suacoco, Gbanga Central Province, Daniel & Barker 220 (BR 901694); 3 miles NE Suacoco, Gbanga, Central Province, Daniel &Barker 418 (BR901740) - NW 0710: Bong Range, Voorhoeve 15 (WAG) - NW 0810: Along the road from Kolahun to Vollaquisi, Jansen 2012 (BR807306). SIERRA LEONE: NW 0811: Rowala, Thomas 1073 (BR 837237). CHARACTERS AND STATES IN THE MORPHOLOGICAL MATRIX USED FOR THE CLADISTIC ANALYSES 1. GROWTH HABIT 1. Erect herb, often somewhat woody at the base 2. Straggling herb, sometimes with erect stems 3. Small subshrub with rheophytic adaptations 4. Shrub or tree 2. STIPULES 1. 2-3 setae or lobes, sometimes simple at the lower nodes 2. Undivided 3. PETIOLE 1. Nearly absent 2. Clearly present 4. HAIRS ON UPPER SURFACE LAMINA 1. Stiff, adpressed multicellular hairs 2. Long, setiform multicellular hairs 3. Absent 5. EMERGENTIA ON LEAF SURFACE 1. Absent 2. Present 6. LEAFINDEX 1. Less than 3 2. Between34 3. More than 6 Note: Leaf index is determined by lengtwwidth ratio. 7. INFLORESCENCE 1. Many-flowered 2. Few-flowered 8. CALYXLOBES 1. Linear 2. Foliaceous - spathulate 9. SETOSE HAIRS ON CALYX LOBES 1. Present 2. Absent 10. COROLLATUBE 1. Small 2. Large 11. HAIRS ON EXTERNAL COROLLA 1. Present 2. Absent 12. DISC 1. Entire 2. Two separated cones Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 zyxwvuts APPENDIX 2 zyxwvutsr zyxw zyxwvutsrq zyxw zyxw zyxw zyxwvutsr SURVEY OF WRECTARIA 13. NECTAROSTOMATA ON NECTAR DISC 1. Present 2. Absent 17. 14. 18. RUGULATE SEXINE 1. Present 2. Absent 19. POLLEN: P EXOTESTA CELLS 1. Strongly elongated 2. Elongated FRUIT DEHISCENCE 1. Often not complete, o r complete, but the margins of the fruit never folding inwards 2. Complete and the margins of the fruit folding inwards 15. 29 PUNCTIClJLATE THICKENINGS ON OUTER TANGENTIAL WALL 20. POLLEN: E 1. <30 2. >30 21. 16. SURFACE INNER TANGENTIAL WALL 1. Smooth 2. Puncticulate POLLEN: P/E 1. <1.20 2. >1.20 APPENDIX 3. MORPHOLOGICAL MATRIX WITH CHARACTERS OF APPENDIX2 1 V angustifolici V belingana V herbacoursi V major V multiflora C: pmcumbens V salicoides V tenella Tamridaea 2 3 4 3 2 1 & 2 1 2 2 1 1 1 2 2 1 1 & 2 2 1 1 1 2 2 2 2 2 1 3 1 1 3 2 1 2 2 4 2 1 3 5 1 2 1 2 2 1 1 1 ? 6 7 1 3 2 1 2 2 2 1 1 2 1 1 2 3 1 1 2 2 1 8 9 1 2 1 2 1 1 1&22 1 1 2 2 1 2 1 1 ? 2 10 11 12 13 14 15 16 17 18 19 20 21 1 2 2 2 2 1 2 1 2 1 1 2 1 2 1 1 2 ? 2 2 1 2 2 2 ? 1 2 1 1 2 1 1 1 1 1 1 1 1 2 1 2 1 1 2 1 2 1 1 1 1 2 ? 1 1 1 1 2 1 1 1 1 2 1 1 1 2 1 2 1 ? 2 1 1 2 2 2 2 1 ? ? 2 1 1 2 1 2 1 ? ? 2 2 2 1 1 1 2 ? ? 1 1 2 2 2 2 1 ? ? 1 Downloaded from https://academic.oup.com/botlinnean/article-abstract/137/1/1/2557149 by guest on 07 June 2020 1. Present 2. Absent 1. >40 2. <40