A nonet of novel species of Monanthotaxis (Annonaceae) from around Africa

Abstract As part of an ongoing revision of the genus Monanthotaxis Baill. (Annonaceae), nine new species are described and one variety is reinstated to species rank. Two new species from West Africa (Monanthotaxis aquila P.H.Hoekstra, sp. nov. and Monanthotaxis atewensis P.H.Hoekstra, sp. nov.), four new species from Central Africa (Monanthotaxis couvreurii P.H.Hoekstra, sp. nov., Monanthotaxis latistamina P.H.Hoekstra, sp. nov., Monanthotaxis tripetala P.H.Hoekstra, sp. nov. and Monanthotaxis zenkeri P.H.Hoekstra, sp. nov.), one new species from Tanzania (Monanthotaxis filipes P.H.Hoekstra, sp. nov.), one new species from the area around Maputo (Monanthotaxis maputensis P.H.Hoekstra, sp. nov.), one new species from the Comoro Islands (Monanthotaxis komorensis P.H.Hoekstra, sp. nov.) and Monanthotaxis klainei (Engl.) Verdc. var. angustifolia (Boutique) Verdc. is raised to species level leading to the replacement name Monanthotaxis atopostema P.H.Hoekstra, nom. nov. (not Monanthotaxis angustifolia (Exell) Verdc.). Complete descriptions, comparisons with related species, ecological information and IUCN conservation assessments are given for the new species. Five species were classified as critical endangered, two species as endangered, one as vulnerable and one as least concern, warranting the need of further collecting and studying those species.


Introduction
Th e genus Monanthotaxis Baill. belongs to the tribe Uvariae in the family Annonaceae . Species of Monanthotaxis are scandent shrubs or lianas, and are confi ned to tropical Africa and Madagascar. Th e generic circumscription of the genus has seen considerable changes in the past. Th e genus was described by Baillon (1890) based on the presence of a single whorl of six petals, and a single whorl of stamens. Most species of Annonaceae typically have two whorls of three petals, and many whorls of stamens. Baillon (1890) named the genus Monanthotaxis after these characteristics (in Greek mono = one, anthir = stamen, taxis = order). In the following 60 years three additional species were described in the genus Monanthotaxis that displayed these generic characteristics. Th en, Verdcourt (1971) synonymized the genus Enneastemon Exell and the African species of the genus Popowia Endl. into Monanthotaxis based on their similarity. Species of Popowia only diff ered from Monanthotaxis by having the petals in two whorls, however species of Enneastemon have the petals intermediate between Popowia and Monanthotaxis, which is a single whorl at the base of the fl ower, and in two whorls apically. With the rise of molecular phylogenetic analyses it has appeared that the genus Friesodielsia is polyphyletic, with most of the African species being sister to the genus Monanthotaxis Richardson et al. 2004;Wang et al. 2012). Further data sampling has also revealed that the monotypic genus Exellia is nested in Monanthotaxis.
Alongside a molecular phylogenetic analysis of Monanthotaxis and related genera, a taxonomic revision of the genus is being undertaken. Th is revision has revealed nine new species of the genus Monanthotaxis which are described in this article. Two are from West Africa, four from western Central Africa, one from Tanzania, one from Southern Mozambique and one from the Comoros. Th is follows a general pattern in recent revisions of both Annonaceae and other tropical African forest taxa that most new species are found in western central Africa and Tanzania (e.g. Bissiengou et al. 2013;Breteler and Wieringa 2008;Breteler 2010;Couvreur et al. 2006;van der Burgt et al. 2015;Wieringa and Mackinder 2012). Also Madagascar is an area with many undescribed species, this is also true for Monanthotaxis, at least seven species will be described in another paper. It is striking that all species here described (except M. fi lipes) had already been collected at least 40 year ago, some even more than 100 years ago. Although of many of them only recently good fl owering material became available, this does prove the importance of herbaria, and the need for exploring their collections (Bebber et al. 2010). Each of these species belongs clearly to the genus Monanthotaxis, as they share the following morphological characteristics with all other species: a climbing habit, glaucous leaves, loosely coherent fl oral chambers, and moniliform monocarps. DNA sequences have confi rmed their phylogenetic position within Monanthotaxis, and these analyses will be published soon in a separate paper with the new generic delimitation of Monanthotaxis (Guo et al. in press). With the species described here, the current number of species of Monanthotaxis will raise to 67.

Material and methods
Over 2000 collections of Monanthotaxis, Exellia, Gilbertiella and African Friesodielsia were examined from the following herbaria: A, AMD, B, BM, BNRH, BR, BRLU, C, E, EA, FHO, G, GC, K, L, LBV, LISC, LISU, M, MA, MO, NU, NY, P, SRGH, U, US, WAG and YA. All measurements were taken from dried specimens, colours were described based on the collector's information. For the species description the same terminology is being applied as in Hoekstra et al. (2014) with the exception that sterile stamens are called staminodes and the peduncle a sympodial rachis, to be in concordance with other Annonaceae literature (e.g. Endress and Armstrong 2011;Maas et al. 2003). Th e extent of occurrence and area of occupancy were calculated using GeoCAT (Bachman et al. 2011) and preliminary conservation status are proposed following the IUCN Red List Category Criteria (IUCN Standards and Petitions Subcommittee 2016).  (Chatelain et al. 1996).

Monanthotaxis atopostema
Etymology. Aquila is the Latin word for eagle. Th is species is named after my son Arend, the Dutch word for eagle. Aquila is used here as a noun.
Discussion. Th is species belongs to a group of species with bisexual fl owers, ovate fl ower buds and predominantly caulifl orous or ramifl orous infl orescences. Most species of this group have obovate to oblanceolate leaves, whereas this species has oblong to elliptic-oblong leaves, a characteristic shared with Monanthotaxis couvreurii and Mo- nanthotaxis atopostema. For the diff erences between those species see Table 1. Monanthotaxis vogelii (Hook. f.) Verdc. is similar to M. aquila, but diff ers in having obovate to oblanceolate leaves with the secondary veins being straight and only slightly curving upwards near the leaf margin and the petals are shorter. Vegetatively Monanthotaxis mannii (Baill.) Verdc. looks similar to M. aquila, but diff ers in having the infl orescences on the leafy twigs (vs rami-or caulifl orous), and rounded fl ower buds (vs ovate).   Hawthorne & Jongkind (2006: 72); invalid: description in English, no type designated (this termination, although admissible, does not follow recommandation 60D of the ICBN).

Monanthotaxis atewae
Diagnosis. Easily distinguishable from all other Monanthotaxis species by the lanceolate sepals 1 cm long. Resembles M. stenosepala (Engl. & Diels) Verdc., but diff ers in the longer sepals, erect hairs on the leaves and branches, and a larger number of seeds per monocarp.
Distribution. Ghana, Eastern Region, Atewa Range Forest Reserve. Figure 2. Ecology. Forest, in thicket, at 750 m altitude. Phenology. Fruiting in May and June. Conservation status. Proposed IUCN Red List Category: Critically Endangered (CR): B2ab(iii), only known from the Atewa Range Forest Reserve and although it is a protected area, the forest is under threat of bauxite mining and logging (Kusimi 2015;Ntiamoa-Baidu et al. 2000). Furthermore, the species has not been collected in more than 40 years.
Etymology. Named after the Atewa Range Forest Reserve in Ghana, to which this species seems to be endemic.
Discussion. Th is species can easily be distinguished from all other species of Monanthotaxis by the large lanceolate sepals. Th e species is similar to Monanthotaxis stenosepala (Engl. & Diels) Verdc., which also has lanceolate sepals and light brown older branches. However, the sepals of M. stenosepala are 4 to 6 mm vs 10 to 12 mm in M. atewensis and the pubescence and number of seeds is diff erent as described in the diagnosis. Two fruiting specimens from Liberia (Stoop 331 and Adam 26189) closely resemble M. atewensis, but no sepals are present to verify the identifi cation. Furthermore, the monocarps are more densely verrucose and the peduncle is shorter and the pedicel larger than the two specimens of M. atewensis from Ghana. More material or more recent material for DNA extraction is needed to assess the status of those specimens from Liberia.
For now we consider this species an endemic to the Atewa Range. Th is is the fi rst plant species that is endemic to this mountain range. However, for several Upper Guinean endemics (e.g. Dorstenia embergeri Mangenot) this range is their most eastern outpost. Some other plants are only known from these mountains and one or two other localities in Ghana. Th e Atewa Range is home of 3 endemic butterfl y species (McCullough et al. 2007). Th is new endemic urges for a strict protection of this unique mountain chain. Description. Liana; young branches reddish brown with dense ascending reddish brown hairs 0.1-0.2 mm, old branches greyish brown, slightly grooved,. Leaves: petioles 3-5 × 0.8-0.9 mm, slightly grooved, indumentum as branches; lamina 4.5-12.0 × 1.8-4.3 cm, length:width ratio 2.1-2.9, oblong to obovate, base cuneate to rounded, apex acute to acuminate, acumen to 1 cm, chartaceous, discolorous, adaxially glossy green, abaxially light greyish green, adaxially sparsely covered with whitish appressed hairs 0.1 mm, soon glabrescent, abaxially with scattered appressed whitish yellowish hairs 0.1-0.2 mm, , venation eucamptodromous, secondary veins 7-11, from base curving upwards, tertiary venation scalariform sometimes obscure. Infl orescences caulifl orous, ramifl orous or axillary, composed from a two-fl owered rhipidium in the axils of the leaves to many-fl owered clusters on the trunk; sympodial rachis 1-15 mm; fl owering pedicels 4-20 × 0.2-0.6 mm, with scattered ascending to erect hairs 0.1 mm; lower bracts strongly reduced or wanting; upper bracts wanting; fl ower buds ovate. Flowers bisexual; sepals 3, 0.8-0.9 × 0.9-1.0 mm, triangular, apex acute, with dense yellowish hairs; receptacle fl at, 1.2-2.0 mm in diameter; petals light yellow to white, in two whorls of 3, but base of inner petals visible in bud; outer petals, 3.5-5.0 × 2.0-3.5 mm, ellipticovate, outside with dense short yellowish hairs, inside with a few hairs near the margins; inner petals 3.0-4.5 × 1.2-1.5 mm, elliptic to narrowly ovate, outside with yellowish hairs at the apex and at the centre, inside glabrous or with a few hairs at the margins; stamens 13-15 in one whorl, connate at base, linear-obconic 0.8-0.9 mm, fi laments 0.4 mm, anther cells lateral to extrorse, connective papillose, truncate, rounded from above, staminodes 0; carpels 9-12, 1.2-1.3 × 0.3-0.4 mm, subcylindric to ellipsoid, dense hairy, with 4 lateral ovules, stigma subsessile 0.2 mm, globose, glabrous. Fruits: Not seen, but according to collection Farron 7359 with 4 articles.  increase of human population around the reserve intensifi es the pressure on the forest, while the surrounding forests are increasingly degrading (Sassen and Jum 2007), warranting the critically endangered status of this species.

Monanthotaxis couvreurii
Etymology. Named after Th omas L.P. Couvreur, a passionate Annonaceae systematist and collector of the type of this species and of Monanthotaxis latistamina P.H.Hoekstra also described in this article. Discussion. Th is species belongs to a group of species with predominantly ramifl orous infl orescences, bisexual fl owers and ovate fl ower buds and looks vegetatively very similar to M. aquila and M. atopostema. For the diff erences between these species see Table 1. M. couvreurii can be distinguished from all Monanthotaxis species in having the stamens basally connate (see fi gure 4F). Monanthotaxis klainei (Engl.) Verdc. also has the stamens connate in one whorl, but in that species the stamens are alternating with staminodes. Diagnosis. Th is species is similar to Monanthotaxis trichantha (Diels) Verdc. because of the dense yellow short indumentum on the young stems. It diff ers in the pendulous fl owers on fi liform pedicels, and in the outer petals covering the inner petals in bud.
Distribution. Tanzania, Lindi Region. Figure 7. Ecology. Steep escarpment with dense thicket, stony-gravelly soil at 700 m altitude. Phenology. Flowers collected the 7 th of February. Conservation status. Proposed IUCN Red List Category: Critically Endangered (CR): B2ab(ii, iii), only known from one collection in the Rondo Forest Reserve in South-east Tanzania. Although it occurs in a forest reserve, satellite images provided by Google Earth (assessed May 2016) show that a major part of the forest in the reserve systematically has been removed, and forest cover is declining over the years.

Monanthotaxis komorensis
Phenology. Flowering from November to January, fruits collected in January and April. Discussion. Th is is the only known species of Monanthotaxis on the Comoros and Mayotte. It is easily distinguished from almost all other Monanthotaxis species by having 6 staminodes alternating with 6 stamens, all in a single whorl. Th e only other species sharing that feature, viz. Monanthotaxis congoensis Baillon and M. paniculata P.H.Hoekstra are very diff erent. Th ese have a single whorl of petals (vs two whorls in M. komorensis), infl orescences of raceme-like or panicle-like rhipidia, their young branches are densely covered with yellowish brown short hairs and they occur in Central Africa. Th e fl owers of Monanthotaxis glaucocarpa (Baill.) Verdc., a species from Madagascar, are not known. Th is species diff ers from M. komorensis in having longer pedicels (>30 mm vs 9 mm), longer stipes (7-9 mm vs 2.0-2.5 mm) and longer and bigger seeds (12-15 mm vs 6 mm). Further, the leaves are less elongate and the young branches are glabrous. Diagnosis. Closely related to Gilbertiella congolana Boutique by the papillose petals and stamens. Diff ers from G. congolana by having 6 oblong stamen (vs 12 linear stamen) which are wider than deep (vs rounded in cross-section).
Ecology. Evergreen forest and forest on shallow soil at summit of hill, elev. 519-1017 m. Although the species has quite a wide distribution, it is only known from four collections, one of which is from a protected area. Discussion. Th is species is similar to Gilbertiella congolana Boutique from Congo (Kinshasa), but it diff ers in stamen number and form, furthermore Monanthotaxis latistamina has thicker petioles, while the petioles of G. congolana are more slender (Table 3).
Although M. latistamina is similar to G. congolana we do describe it in Monanthotaxis as Gilbertiella Boutique will be synonymized with Monanthotaxis. Boutique (1951) described Gilbertiella based on linear stamens, outer petals that cover the inner petals in bud only at the apex, and an apical appendage on the inside of the petals. Th ese characters on their own occur in other species of Monanthotaxis as well. Th e outer petals overlapping the inner petals only at the apex occurs in a quarter of all Monanthotaxis species, the linear stamens occur in some species such as Monanthotaxis fi lamentosa (Diels) Verdc. and Monanthotaxis maputensis P.H.Hoekstra (fi gure 11) and a more or less developed appendage on the petals occurs in species such as Monanthotaxis le-testui Pellegrin and male fl owers of Monanthotaxis caulifl ora (Chipp) Verdc. and often in young fl ower buds. All other characteristics of Gilbertiella congolana are typical or at least normal for Monanthotaxis, such as having only a few stamens in one whorl and uniseriate stipitate monocarps. Also Walker (1971) reported a strong affi nity between Monanthotaxis and Gilbertiella based on the microbaculate pollen exine. Based on all these similarities we place Monanthotaxis latistamina in the genus Monanthotaxis. Furthermore, DNA sequences confi rm the placement of Monanthotaxis latistamina within the genus Monanthotaxis (Guo et al. in press).
Th e specimen of Monanthotaxis latistamina from the Republic of Congo has some diff erences with the three specimens from Gabon. Th e fl ower buds and stems of the specimen dried very blackish and the leaves are coriaceous and greyish vs chartaceous and green in the Gabonese specimens. However the distinguishing characteristics with G. congolana are the same as with the Gabonese specimens. More collections are needed to verify if this is just an aberrant collection or a diff erent (sub)species. For now this collection is retained as belonging to M. latistamina based on the similarities in fl owers and stamen, but it is excluded as a paratype. Diagnosis. Closely related to Monanthotaxis caff ra (Sond.) Verdc., but diff ers in having long fi laments which occupy more than half of the total stamen length, while M. caff ra has short fi laments and the anther cells occupy more than half of the total stamen length. Further M. maputensis has shorter and less hairy leaves, the fruiting pedicels are more slender and the stipes are shorter than with M. caff ra.
Distribution. From just South of the border of South Africa and Mozambique north to 23 degrees in the province Inhambane in Mozambique. Figure 12.
Ecology. Occurring in diff erent types of thickets and forests on sandy soils, at 0-150 m altitude.
Phenology. Flowers collected in November, December and February to April, fruits collected from March to September.
Conservation status. Proposed IUCN Red List Category: Least Concern (LC): EOO 43433 km 2 , AOO 128 km 2 . Within the distribution range it has been collected from more than 10 diff erent localities and at least 3 nature reserves. Furthermore it is quite common in the coastal dunes of Mozambique, therefore we suggest the status of Least Concern for this species.
Etymology. Named after the town and province Maputo, the center of the distribution and where most collections originate from.
Additional specimens examined (all paratypes, except when noted as excluded). MOZAMBIQUE. Gaza: Macia-Messano, 28 Aug 1980, A. Nuvunga   Diagnosis. Diff ers from other Monanthotaxis species in having bisexual fl owers with three thick outer petals, and wanting or strongly reduced inner petals. Th e other species of Monanthotaxis with three petals or reduced inner petals have unisexual fl owers, such as Monanthotaxis diclina (Sprague) Verdc. and Monanthotaxis caulifl ora (Chipp) Verdc.
Etymology. Named for the three petals, one of the diagnostic characteristics of this species.
Additional specimens examined (all paratypes Discussion. Th is species can easily be distinguished from all other Monanthotaxis species by the small bisexual fl owers with 3 outer petals and wanting to strongly reduced inner petals. Some other species exist, such as Monanthotaxis caulifl ora (Chipp) Verdc., Monanthotaxis diclina (Sprague) Verdc. and Monanthotaxis mortehanii (De Wild.) Verdc., which have reduced inner petals, but those have unisexual fl owers. Another probably new species from Cameroon which is currently still under study, also has completely wanting inner petals, but also that species has unisexual fl owers.
Th e type specimen from Cameroon has refl exed and thickened edges at the leaf base (e.g. fi gure 13B), which is wanting in the specimens from Gabon, where only a slight depression can be seen next to the petiole insertion. Th is character is variable in other species as well, such as Monanthotaxis schweinfurthii (Engl. & Diels) Verdc. Th e very distinctive, small fl owers with only 3(-4) petals in the Gabon specimens make these specimens belong to M. tripetala.
Th e specimen of Moungazi 252 has a gall on one of the branches, which has not been observed in any of the currently collected material of the Monanthotaxis species, while the collection of Wieringa 8229 has many brown velvety galls on one of the leaves (WAG spirit collection). Th e latter type of gall has been observed in other Monanthotaxis species in Central Africa.

Diagnosis.
Th e only other two species of Monanthotaxis with the anther cells convergent apically hiding the connective are Monanthotaxis bicornis (Boutique) Verdc. and M. fi lamentosa (Diels) Verdc., it diff ers from both in having small fl owers and further can be distinguished from the fi rst by the almost glabrous leaves with cuneate base and having only 15 stamens, while M. fi lamentosa has long erect hairs on the stems and pedicels and has ovate to ovate-lanceolate fl ower buds with much longer petals.

Ecology. Forest.
Phenology. Flowering in October. Conservation status. Proposed IUCN Red List Category: Critically Endangered (CR): B2ab(iii), only known from the type collection, which was collected more than a hundred years ago in an unprotected area. Actually, the species may well be extinct already.
Etymology. Named after G.A. Zenker, who collected many specimens of Monanthotaxis in Cameroon from the end of the 19 th and the beginning of the 20 th century. Th e types of seven species of Monanthotaxis were collected by him.
Discussion. Sprague and Hutchinson (1916) noted that they had seen the specimen Zenker 3495a, but felt reluctant to describe it because of the immature fl owers on the specimens in the Kew herbarium. However, the fl owers are fully developed on the specimens of G and HBG where the fl owers are open, some of which have lost the petals already.
M. zenkeri is one of three species of Monanthotaxis with anther cells converging at the apex of the stamen. It can be distinguished easily from the other two species by the small fl owers and dense short erect hairs on the young branches and leaves (Table 5). Vegetatively, this species is quite similar to Monanthotaxis diclina (Sprague) Verdc. which also is densely covered with short reddish brown hairs. However, the fl owers are very diff erent, M. diclina has unisexual fl owers, the female infl orescences are caulifl orous and the male infl orescences axillary. Furthermore, the stamens are very diff erent as M. diclina has 6 stamen in one whorl with the anther cells latrorse and an external whorl of 12 staminodes.