Revision of the African genus Crotonogyne ( Euphorbiaceae )

The African genus Crotonogyne was described in 1864 by Müller Argoviensis with one species, C. manniana Müll. Arg. from the island Bioko of Equatorial Guinea. Baillon (1891) described the second species, a rheophyte from Gabon, but placed it in Manniophyton. Pax (1894, 1897, 1899) and Prain (1911, 1912a, 1912b, 1912c) published most of the 23 specific names available (Govaerts et al. 2000). Pax & Hoffmann (1912) classified it in the subfamily Crotonoideae, tribe Chrozophoreae in a group of genera with an irregular 2–3-lobed male calyx. In the same publication they subdivided Crotonogyne into Crotonogyne s. str. with free male petals, counting two species, the type species C. manniana and C. preussii Pax, and a separate genus Neomanniophyton with male petals fused at the base for the remaining 12 species. Because Crotonogyne manniana has in fact fused male petals, Prain (1913) correctly observed that Neomanniophyton is superfluous. For Crotonogyne preussii, the second species of Crotonogyne s. str., he suggested, eventually, a sectional position as an adequate recognition. Pax (1914) however, reduced Neomanniophyton to a subgenus of Crotonogyne and wrongly transferred C. manniana to it. Webster (1994) placed Crotonogyne in the subfamily Acalyphoideae, tribe Aleuritideae, subtribe Crotonogyninae Webster (1975), together with two other African genera Cyrtogone and Manniophyton. Radcliffe-Smith (2001) followed Webster (1994) in his classification of the genus Crotonogyne. The genus has not been revised on an African scale since 1912 when it was treated for the Flora of tropical Africa by Prain (1912c) and in the same year in Das Pflanzenreich by Pax & Hoffmann (1912). Identification of new material collected since proved to be very difficult due to incorrect or incomplete delimitation of the species. A complete revision is therefore undertaken, also as a basis for the treatment of the genus in the Flore du Gabon.


INTRODUCTION
The African genus Crotonogyne was described in 1864 by Müller Argoviensis with one species, C. manniana Müll.Arg. from the island Bioko of Equatorial Guinea.Baillon (1891) described the second species, a rheophyte from Gabon, but placed it in Manniophyton.Pax (1894Pax ( , 1897Pax ( , 1899) ) and Prain (1911Prain ( , 1912aPrain ( , 1912bPrain ( , 1912c) ) published most of the 23 specific names available (Govaerts et al. 2000).Pax & Hoffmann (1912) classified it in the subfamily Crotonoideae, tribe Chrozophoreae in a group of genera with an irregular 2-3-lobed male calyx.In the same publication they subdivided Crotonogyne into Crotonogyne s. str.with free male petals, counting two species, the type species C. manniana and C. preussii Pax, and a separate genus Neomanniophyton with male petals fused at the base for the remaining 12 species.Because Crotonogyne manniana has in fact fused male petals, Prain (1913) correctly observed that Neomanniophyton is superfluous.For Crotonogyne preussii, the second species of Crotonogyne s. str., he suggested, eventually, a sectional position as an adequate recognition.Pax (1914) however, reduced Neomanniophyton to a subgenus of Crotonogyne and wrongly transferred C. manniana to it.Webster (1994) placed Crotonogyne in the subfamily Acalyphoideae, tribe Aleuritideae, subtribe Crotonogyninae Webster (1975), together with two other African genera Cyrtogone and Manniophyton.Radcliffe-Smith (2001) followed Webster (1994) in his classification of the genus Crotonogyne.
The genus has not been revised on an African scale since 1912 when it was treated for the Flora of tropical Africa by Prain (1912c) and in the same year in Das Pflanzenreich by Pax & Hoffmann (1912).Identification of new material collected since proved to be very difficult due to incorrect or incomplete delimitation of the species.A complete revision is therefore undertaken, also as a basis for the treatment of the genus in the Flore du Gabon.

MATERIAL AND METHODS
Classical methods of herbarium taxonomy were followed.This study is based on all Crotonogyne herbarium specimens from the herbaria of BM, BR, BRLU, HBG, K, MA, P, and WAG.The search for lost type material from B (Berlin) was done at the herbaria of BR, HBG, K, and P, and was most succesful at HBG.The selection of a neotype for two names has been done with respect to characters given in the protologues and origin of their types.The Index Herbariorum (Thiers continuously updated) is followed as regards the herbarium acronyms.Specimens cited but not seen are marked with an asterisk.The relevant data of all specimens are stored at the Botany Section of Naturalis, Biodiversity Center, Leiden.All illustrations (figs  are based on herbarium material.Morphological illustrations were prepared from the specimens mentioned in the captions.MAPMAK-ER was used to produce the distribution maps from geolocalized specimens.

Morphology
The habit of Crotonogyne species is a shrub or small tree with lepidote or stellate indumentum (fig.1A-H), in some species (e.g.C poggei) mixed with simple strigose or hispid hairs (fig.1I-K).The stipules are usually not early shed, but they offer no distinctive characters.The alternate leaves have two, sometimes three or even four, distinct glands at the base of the lamina on the upper surface next to the midrib (figs 7F, 11A & 13C), though they are often missing in C. parvifolia.The glands on the lower leaf surface are arranged in a simular pattern for all species (see figs 7A & 13B), except for C. parvifolia where this pattern does not occur or is obscure.In many species, C. caterviflora and C. parvifolia excepted, some leaf laminas are very narrowly attenuate at their base as to form a so-called false or pseudopetiole (e.g.fig.7C) that may reach a length of 5.5 cm in C. micrantha.Leaves with such a pseudopetiole occur mixed with leaves without a false petiole, i.e with true petiole only.The inflorescences are slender, ± erect, scarcely branched, and the male ones may reach a length of more than 1 m.The male flowers are arranged in distant glomerule-like entities (e.g.fig.7B) or in basally branched, densely bracteate spikelets (fig.13D), which are supported by a biglandular (rarely with up to 3 or 4 glands) bracts (e.g.figs 1L & M, 7D, 13D).These glands are missing in C. caterviflora.The female inflorescence is, as a rule, shorter than the corresponding male one.The female flowers are single or a few together, sometimes more or less crowded towards the top of the inflorescence.They are also, C. caterviflora again excepted, supported by a glandular bract as in the male inflorescences.
The question whether the unisexual flowers of Crotonogyne are monoecious or dioecious remains unanswered, at least for most species.Pax & Hoffmann (1912, 1931) and Pax (1921) described the genus as dioecious and Prain (1912c) noted that the flowers are "dioecious, rarely casually monoecious".Léonard (1962) described Crotonogyne individuals as monoecious or dioecious, and Radcliffe-Smith (2001) as dioecious rarely monoecious.Herbarium specimens did not give sufficient information to answer this, the branches were either male or female, even when mounted together on the same sheet.Only a few collectors gave useful information about this problem.The fieldnotes of D. Thomas 105 and 2550, pertaining to C. neglecta, state "monoecious", and Leeuwenberg 6437, a C. poggei collection, says "treelet with male and female flowers".The fieldnotes of Wieringa et al. 4701, a collection of C. gabunensis, men-tion male and female shrubs, but those of Mc Pherson 15551 of the same species state monoecious, as Letouzey 10344 for C. zenkeri.Of the latter species Bos 5732 notes "shrub not strictly dioecious, but producing usually one sex at the time" and of Bos 4364 of the same species, "dioecious, but also bisexual plants, flowers always on different inflorescences".The WAG specimen of this last collection shows a branchlet with a female inflorescence and also an impoverished male one.Prain (1912c) in his description of C. zenkeri noted that "casually male and female racemes on the same branch, and casually a solitary female flower at base of the male raceme".And about the male flowers in spikelets arranged in separate glomerules he stated that "the rarely simply glomerulate arrangement of male flowers may be provided with a solitary central female flower accompanying each glomerule".The latter situation has not been observed in the material investigated for this revision.In conclusion it may be stated that Crotonogyne individuals may be bisexual or unisexual, or are producing only one sex at the time, or at least on different branches.The bisexual status is most likely for C. neglecta and C. zenkeri individuals.
The flowers of Crotonogyne are basically mostly 5-merous, although mixtures of 4-and 5-merous flowers do occur in some species (e.g. C. gabunensis) in the same specimen.C. micrantha has only 4-merous flowers, but this species is only known from two collections.The calyx of the male flowers opens by splitting into 2-3(-5) parts.The male petals, 4-6(-7) in number, are free or united, only in their basal part or ± completely so in C. zenkeri (fig.23B).In C. poggei the petals are as a rule united at their base, but free petals have a few times been observed.The extrastaminal disc consists of 5-8, usually free lobes.The number of stamens varies between 6 in C. preussii and 28 in C. giorgii.They may be ± free or more or less united into a short androphore as in C. poggei, C. preussii and C. zenkeri (e.g.fig.19A, 21A, 23A).There is no pistillode.The female flowers have a long pedicel.The sepals, 4-5 in number, are usually united at base and may be provided by a single large gland in the sinus between the lobes (fig.5A) or more or less, usually smaller, on the margin (fig.23D).Once, in C. poggei, shortly stalked glands have been observed.The female sepals of C. micrantha are ± free and biglandular at base.The petal number in the female flowers varies between 4 and 6, they are always free.The female disc is annular to more or less cupular.The three styles are short, they are unforked in C. manniana (fig.11G), but at least once to several times forked in the remaining species, producing few to many stigmas.The fruit is a 3-seeded capsule.The seeds are glabrous, brown-marbled.

Chorology and ecology
The eleven species of Crotonogyne are all confined tot the Guineo-Congolian forest region (White 1979) (fig.2).The type species Crotonogyne manniana is restricted tot the island Bioko of Equatorial Guinea and has not been collected since Mann collected it for the first time in 1860.All other species, Crotonogyne micrantha and C. parvifolia excepted, are more widely distributed over the forest area.Crotonogyne poggei is the most wide-spread species, ranging from eastern Nigeria in the West to Kasai (D.R. Congo) in  the South and the Central African Republic in the East.In Upper Guinea Crotonogyne caterviflora is the only species present, the other ten species all occur in Lower Guinea and Congolia.The highest diversity of Crotonogyne is found in Cameroon with seven species of which C. micrantha and C. zenkeri are endemic.Equatoral Guinea comes next with four species.In the remaining countries the genus is represented by three species only.Species of Crotonogyne are found in primary or old secondary rain forest, mostly on dry land with two exceptions.Crotonogyne parvifolia, an endemic species of Gabon, is a rheophyte and has only been collected in river beds and C. giorgii which is mostly found in marshy sites and in periodically inundated forests

Fig. 7 .
Habitat and distribution -Primary to old secondary forest in Cameroon, Equatorial Guinea (Rio Muni), Gabon, and Breteler, Revision of Crotonogyne (Euphorbiaceae) Jun.1966, Sita 1359 (BR, P); Fôret de Mayumbe, Jan. 1891, Thollon 4006 (P).Notes -The type of Crotonogyne angustifolia can only be distinguished from C. gabunensis by its narrow leaves.These are, altough rare, also present in the latter species and, moreover, are linked by intermediate sizes tot the more commonly occuring broader leaves in C. gabunensis.Prain (1911) characterised his Crotonogyne lasiocarpa by the 4-merous female flowers with 7-8-parted styles.Tetra-merous female flowers are frequently seen in Crotonogyne ga-bunensis and may even occur mixed with 5-merous ones in the same inflorescence as observed in Wieringa et al. 4701.

Figure 11 - 5 .
Figure 11 -Crotonogyne manniana: A, petiole with glands; B, male flower; C, male corolla, D, androecium with disc glands; E & F, anther from inside and outside; G, female flower, petals fallen off.A-F after pencil drawing at K made by Mr Smith from Mann 220; G from Mann 219 (K).Scale bar = 5 mm.Drawn by H. de Vries.

Figure 13 -
Figure 13 -Crotonogyne micrantha: A, male flowering branch; B, detail of leaf underneath showing gland; C, leaf axil with stipules and petiole with glands; D, group of male spikelets with glandular bract; E, male flower bud; F, male flower; G, scales; H, female flower with reflexed petals; I, female flower, one sepal and two petals removed; J, female sepal from outside; K, young fruit.A & D from W.J. de Wilde c.s .2186(WAG); B, C & E-K from Letouzey 12295 (P).Scale bars: A = 10 cm; B, D-F & H-K = 1 mm; C = 1 cm; G = 0.3 mm.Drawn by H. de Vries.