Revision of the African genus Uvariastrum (Annonaceae)

Abstract The genus Uvariastrum (Annonaceae) is restricted to continental Africa and is characterized by sepals with folded margins, few carpels and numerous stamens. The genus is mainly found in the tropical lowland rain forests of Africa, with one species growing in a drier woodland habitat. The species name Uvariastrum pynaertii De Wild is reduced into synonymy with Uvariastrum zenkeri Engl. & Diels. Uvaraistrum neglectum Paiva and Uvariastrum modestum Dielsare transferred to the genus Uvaria leading to two new combinations: Uvaria modesta (Diels) Couvreur, comb. nov. and Uvaria paivana Couvreur, nom. nov. Five species are currently recognized in Uvariastrum. The present revision, the first of the genus for over 100 years, provides an overview of previously published information and discussions on morphology, taxonomy and palynology. Preliminary conservation status assessments are provided for each species, as well as diagnostic keys for fruiting and flowering material as well as detailed species descriptions. Furthermore, all species are illustrated by line drawings and all species are mapped.


Introduction
Annonaceae (Magnoliales) is a pan tropical family of trees, shrubs and lianas and represent an important component of tropical rain forest ecosystems worldwide (Chatrou et al. 2012). Africa contains 42 genera and around 400 species (Couvreur 2011;Couvreur et al. 2012). Recently, a series of publications have contributed to a better understanding of African Annonaceae (Botermans et al. 2011;Couvreur 2009;Kenfack et al. 2003;Luke and Deroin 2005;Versteegh and Sosef 2007) as well as a dedicated scratchpad page (afroannons.myspecies.info). Uvariastrum Engl. & Diels belongs to the sub family Annonoideae Raf. and tribe Monodoreae Baill . (Chatrou et al. 2012). Th is tribe contains ten other African genera whose phylogenetic relationships were elucidated by Couvreur et al. (2008b). Uvariastrum was recovered with strong support as sister to another African genus Hexalobus A.DC., these in turn sister to the East African genus Asteranthe Engl. & Diels (Chatrou et al. 2012;Couvreur et al. 2008b).
Uvariastrum is a genus of fi ve species restricted to lowland tropical rain forests across Africa expect for Uvariastrum hexaloboides (R.E.Fr.) R.E.Fr. that is found in drier woodlands of southern Democratic Republic of Congo (Katanga region) and northern Zambia. Gabon appears as a center of diversity with four of the fi ve species occurring there.
Uvariastrum are medium sized trees or shrubs as most of the members of the tribe Monodoreae. Th e trunks of Uvariastrum never present buttresses, can be fl uted when old, but are generally straight and cylindrical. Th e phyllotaxis is distichous as usual for Annonaceae. Th e leaves show the typical Annonaceae pattern: they are simple, entire, distinctly petiolate, and exstipulate. Interestingly, leaves alone can be very useful for species identifi cation (see key below and Fig. 1). Two species, U. insculptum Sprague & Hutch. and U. hexaloboides , have pubescent leaves, even in older individuals, especially along the upper side of the midrib. Besides their geographical disjunction, the former has clearly impressed venation above (Fig. 1C) and the latter has an emarginated leaf apex (Fig. 1E). Th e three other species of Uvariastrum can be distinguished by the size and shape of the leaves, the length of the petiole and the insertion of the lamina on the petiole. Uvariastrum zenkeri Engl. & Diels (Fig. 1A) has large leathery leaves and the lamina is inserted on top with a petiole length 2-4 mm long. Both U. germainii Boutique and U. pierreanum Engl. have the lamina inserted on the side and forming a groove, but the former (Fig. 1D) has characteristic small, long-apiculate leaves with long petioles (4-7 mm) whereas U. pierreanum (Fig. 1B) has slightly longer leaves with a short apiculate apex and shorter petioles (2-4 mm). Th e midrib is sunken to fl at on the upper side which is the common state for African Annonaceae. Only a few African genera ( Isolona Engler, Monodora Dunal and Ophrypetalum Diels) have raised midribs which provides a useful taxonomical indication in sterile material (Couvreur 2009). Th e midrib is always prominent on the lower side. Secondary venation is brochidodromous, i.e. secondary veins joined together at the margins in a series of arches (loop-forming). On the upper side the venation is either raised ( U. germainii , Figure 1. Leaf and petiole morphology in Uvariastrum . a U. zenkeri ( Bergen 335 , WAG) b U. pierreanum ( Jongkind 7318 , WAG) c U. insculptum ( Staudt 740 , M) d U. germainii ( Ndolo Ebika 311 , WAG) e U. hexaloboides ( Schmitz 12046 , WAG). U. pierreanum ), clearly impressed ( U. insculptum ) or not very prominent ( U. hexaloiboides , U. zenkeri ). Th e tertiary venation is always reticulate.
Th e basic infl orescence type in Annonaceae is a thyrsoid (Weberling and Hoppe 1996): a cymosely branched partial infl orescence on a multinodate main axis, ending in a terminal fl ower (determinate). Th is sort of infl orescence is also called a rhipidium. In Uvariastrum , the infl orescences are defi ned as a single-fl owered rhipidium developing from the axillary meristem similar in structure to those of Isolona (Couvreur 2009). Sometimes additional single fl owered rhipidia develop from extra-axillary meristems. In U. zenkeri , U. pierreanum , and to a lesser extent in U. hexaloboides , caulifl ory has been observed in which case there are numerous clustered fl owers on main stems (Fig. 2d). Th e bracts vary from 1-3 being semi-amplectent on the petiole and caducous. Th ey are generally small varying from 1-10 mm in length. Large leaf-like bracts, like for example those in Isolona caulifl ora Verdc., have not been recorded in the genus.
Flowers in Uvariastrum are actinomorphic, cyclic, trimerous with one whorl of three free sepals and two whorls of three free petals each (referred to as outer and inner), and bisexual, conforming to the general pattern found within Annonaceae (van Heusden 1992). Th e pedicel is generally long varying from 0.5-5 cm, and is glabrous to densely pubescent. Th e bracts are inserted at the base of the pedicel, ranging from 1-3, short, 1-7 mm long, generally falling off early and leaving a scare, pubescent outside and glabrous inside.
Th e sepals are large varying in shape and qualifi ed as reduplicate-valvate (van Heusden 1992) in bud meaning the margins are curved outwards (Fig. 2 e). Reduplcatevalvate sepals are found in several other genera and have been linked to large fl ower buds (van Heusden 1992). Within the tribe Monodoreae this character is also found in the genus Mischogyne Exell (see below) and has been observed to a slighter degree in Asteranthe Engl. & Diels (Couvreur, pers. obs.). Th e sepals enclosing the rest of the fl ower until anthesis is a character shared with the sister genus of Uvariastrum , Hexalobus (Botermans et al. 2011). Th e inner and outer petals are sub-equal in length, the inner ones slightly shorter, with a valvate aestivation. Th e petals of Uvariastrum are not fused in sharp contrast to Hexalobus and several other genera from the tribe (e.g. Isolona , Monodora, Asteranthe , Sanraphaelia Verdc.) (Couvreur et al. 2008b).
Th e androecium has numerous extrose stamens conforming to the typical Annonaceae confi guration (Fig. 2g). Th e disposition of anthers in Annonaceae fl owers is still poorly known and more data is needed to better understand this (Endress and Armstrong 2011). Th e fi laments are generally very short and wide. Th e connective is discoid, glabrous to densely pubescent; e.g., U. insculptum (Fig. 3a). In U. germainii the center of the connective is adorned by a protuberance termed umbonate (Maas et al. 2003) or tongue shaped, a character also found in other species like Uvaria angolensis Welw. ex Oliv. (Le Th omas 1969) and species of Annickia Setten & Maas (Versteegh and Sosef 2007) or Greenwayodendron Verdc. (Couvreur et al. 2009). Carpels are free, varying from 1-15 and are densely pubescent. Th e stigma is bilobed, or capitate in U. pierreanum , and can be glabrous or pubescent. Ovules vary from 15 to numerous and are biseriate with a parietal placentation.    ( Breteler 5811 ) b pollen grain of U. insculptum ( Breteler 5811 ) c pollen grain of U. germainii ( Lebrun 5977 ) d pollen grain of U. hexaloboides ( Breteler 11894 ) e pollen grain of U. zenkeri ( Bos 6266 ) f Pollen grains of U. zenkeri in connective shield ( Bos 6266 ). Couvreur et al. (2008a) undertook a palynological analysis of fi ve genera from the Monodoreae tribe: Asteranthe , Hexalobus , Isolona , Monodora and Uvariastrum . A short overview is provided here (Fig. 3). Uvariastrum has pollen in acalymmate, tetragonal tetrads with constituent monads inaperturate. Th e size of the tetrads ranged from 52-107 mm in diameter. Based on the exine ornamentation a single pollen type was recognized being regulate or psilate resulting in a very homogenous genus. Th is contrasts to the closely related genus Hexalobus with a similar number of species (Botermans et al. 2011) but with three diff erent types of pollen ornamentation (granular to gemmate; areolate-verrucate to/or regulate; or psilate with perforations).

Taxonomic history
Th e fi rst species name later to be accommodated into Uvariastrum was Uvaria insculpta Engl. & Diels (1899). Two years later in their " Monographien afrikanischer Pfl anzen-Familien und -Gattungen Anonaceae " (Engler and Diels 1901) Engler described the genus Uvariastrum which included one species: Uvariastrum pierreanum . Uvariastrum zenkeri was described a few years later (1907) followed by U. pynaertii De Wild. that is now considered a synonym of it. Uvaria insculpta was later transferred into Uvariastrum by Sprague and Hutchinson (1916). Uvaristrum was distinguished from Uvaria by its tree or shrub habitat ( Uvaria species are lianas), simple hairs ( Uvaria having generally stellate hairs), valvate petals and few carpels (less than 6), even though Uvariastrum pierreanum can have up to 10 carpels. Sprague and Hutchinson (1916) transferred the species name Uvaria elliotianum Engl. & Diels into Uvariastrum based on its valvate sepals and petals with an indumentum of simple hairs. In 1953, Robert E. Fries (Fries 1953) transferred Uvariastrum elliotianum into the genus Mischogyne , described a few years earlier based on the stamens inserted along the receptacle and the lack of a fl at discoid connective appendage on the stamens. Th is was also followed by several authors (Hawthorne and Jongkind 2005;Le Th omas 1969) and confi rmed based on molecular data (Chatrou et al. 2012;Couvreur et al. 2008b). Fries (1953) also described Uvaria hexaloboides R.E.Fr. which he later transferred to Uvariastrum and was accepted by subsequent authors including here (Robson 1960;Verdcourt 1971).
As is evident from the above there has been some confusion between the genera Uvaria and Uvariastrum . Th us some species were initially described as Uvaria then transferred into Uvariatsrum . Besides the species discussed above, Engler and Diels (1901) described Uvaria dependens Engl. & Diels which was then transferred into Uvariastrum in 1907 by Diels. I agree with Verdcourt (1971) that this species belongs to Uvaria . I collected it in Tanzania, and besides the fact that it was a liana, it had stellate hairs and a terminal infl orescence, the monocarps were long-stalked (also described in Verdcourt 1971, Fig. 4), a character never found within the tribe Monodoreae (Couvreur et al. 2008b). Th e last two names that are linked to Uvariastrum are Uvariastrum neglectum Paiva and Uvariastrum modestum Diels both from Angola. For both names we only have the type material (which includes fl owers but no fruits) and I think these names are better excluded from Uvarias- trum and placed for now in Uvaria because of their terminal infl orescences and pollen that shed in monads at least for U. modestum (Le Th omas, unpublished data).

Materials and methods
Measurements were made on dried herbarium specimens, although certain characters such as shape were observed on alcohol-preserved fl owers or fruits, as well as fi eld notes and photos. All specimens cited in this paper have been seen by the author (see acknowledgments for list of herbaria). I also used online databases for type specimens in order to provide a complete overview of type distribution (e.g., Global Plants, http:// plants.jstor.org). In cases where the type collection was composed of more than a single sheet without any clear indication that these were part of a series (sheet 1, 2, etc.), a lectotypifi cation or secondary lectotypifi cation was done to designate a single sheet following recommendation of Article 19. Preliminary conservation assessments for each species followed the IUCN recommendations (IUCN 2012) and were based on the distribution of herbarium specimens (Schatz 2002) by calculating the Extent Of Occurrence (EOO) and the Area Of Occupancy (AOO) based on category B (Geographic range). I used the online tool GeoCAT (Bachman et al. 2011) (http://geocat.kew.org/). Th e cell area was always set to the largest permissible value which is just under 10 km 2 (cell diameter = 3.16 km). Setting a cell size diameter at 3.2 km or larger will not allow any taxon to be listed as Critically Endangered where the threshold AOO under criterion B is 10 km 2 (IUCN 2012). Maps were generated with ArcMap 10.0 (ESRI).

Uvariastrum germainii
Distribution. Gabon, Central African Republic, Republic of Congo and Democratic Republic of Congo, mainly in the Congo basin. (Figure 6).
Habitat and ecology. Th is species is found in Gilbertiodendron J.Léonard forests as well as in semi-deciduous forests. One collection indicates a habitat on white sand on a river bank ( Germain 412 ); 400-900 m.
Phenology. Mature fl owers collected from Feb to Mar, Jun, Aug and Oct. Mature fruits collected in Jan, May to Jun and Oct.
Preliminary IUCN conservation status. VUB2ab(iii): Uvariastrum germainii is moderately represented in herbaria, and has an Area of Occupancy less than 60 km² with just nine localities. Although it is found in several protected areas (Dzanga-Sangha, Central African Republic; Nouablé-Ndoki National Park, Republic of Congo) it is highly fragmented in distribution (although this might be linked to collecting eff ort). Th e vulnerable category thus seems applicable. Uses. None recorded. Notes. Th is species somewhat resembles U. pierreanum in the small size of its leaves, but can be distinguished by the longer petioles (4-7 mm vs 2-4 mm), long acuminate leaf apex and tongue-shaped connectives of the stamens. In addition, the fruits of U. germainii are clearly ribbed and glabrous, compared to the smooth and pubescent fruits of U. pierreanum .
Distribution. Southern Democratic Republic of Congo, Katanga region (Lubumbashi), northern Zambia and one collection from the Rukwa region in Tanzania. (Figure 8).
Habitat and ecology. Common in woodland, especially in Brachystegia Benth. and Isoberlinia Craib & Stapf woodlands, on rocky soil, sometimes associated with bright red sandy loam; 1000-1600 m.
Phenology. Mature fl owers found between Oct and Jan, but mainly in Nov to Jan, sometimes fl owering in May. Mature fl owers found in Jul, Sep and from Nov till Dec.
Preliminary IUCN conservation status. LC: Uvariastrum hexaloboides is quite well represented in herbaria but the last collection was made in 1985. Th e area of extent is 128 km² however there are more than 10 localities. Th e species occurs in three protected Forest Reserves in Zambia (Ichimpi, Dome and Luano Forest Reserves) thus the least concern category seems appropriate, although more recent observations will be important to confi rm this assessment. Uses. Th e wood is sometimes used to make arcs ( Gilbert 172 ) Notes. Th is species is easily diff erentiated from all other species of the genus by its densely pubescent leaves (petioles and midribs) combined with emarginate leaf apices (Fig. 1e).
In the protologue of Uvaria hexaloboides , Fries cited two syntypes: 1260 and 1260a, and I select here the former as the lectotype as it was located in several herbaria (UPS and Z).
Distribution. Mainly a West African species, found in Liberia and Ivory Coast, two collections in Cameroon and two in Gabon; Figure 10.
Habitat and ecology. Found in lowland primary and secondary rain forest 0-400 m. Phenology. Mature fl owers found between Oct and Feb. Mature fruits found in Feb and from Apr till May and in Jul.
Preliminary IUCN conservation status. LC: Uvariastrum insculptum is well represented in herbaria and has a large distribution across West Africa, and a few specimens from Central Africa. It is also present in several protected areas such as national parks or protected areas (Taï National Park, Banco National Park, Monogaga Forest Reserve (Ivory Coast); Stubbs Creek Forest Reserve (Nigeria)). Th e Least Concern category thus seems appropriate.

Vernacular names. None known.
Uses. None known. Notes. Th is is the only largely West African species of the genus, although it occurs in the South-West region of Cameroon. It is easily distinguishable by its densely pubescent leaves and midrib and its impressed venation of the upper side of the leaves. Two Staudt collections were cited in the protologue of Uvaria insculpta : n. 740 and n. 900. Although it would appear as if the former was already considered as the lectotype I found no publication formalizing this (e.g., Global Plants), so I have lectotypifi ed it here using because it has several sheets compared to one located for #900.  Description. Tree to 20-25 m high, d.b.h. up to 40 cm; bole cylindrical, old branches spreading, glabrous, truck fl uted when old, bark brown-grey; fi rst year branches sparsely pubescent to glabrous, hairs ca. 0.5-1 mm long, appressed, light brown; leaf buds elongated, pubescent, hairs ca. 1 mm long, appressed, light brown. Petioles 2-4 mm long, 1-1.5 mm in diameter; glabrous, sometimes sparsely pubescent in fi rst year leaves, hairs ca. 0.5 mm long, appressed; leaf lamina inserted on top, weakly grooved adaxially. Leaf lamina 6-12(-16) cm long, 2-4.5 cm wide, length:width ratio 2.5-4.2, narrowly elliptic to elliptic or narrowly obovate to obovate, sometimes narrowly oblong to oblong, papyraceous to sub coriaceous in older leaves, glabrous to sparsely pubes-cent, hairs ca. 0.3 mm long, appressed, light brown; lamina dark green adaxially; light green abaxially; base cuneate to decurrent, apex acuminate, acumen 0.7-2 cm long, lamina margins wavy; midribglabrous on both sides; secondary veins 7-12, curving upwards, arching towards margins, glabrous, slightly raised adaxially; clearly visible abaxially. Raphidia 1-3 on young to old branches, numerous when caulifl orous. Flowering pedicel 1.5-5 cm long, 1-1.5 mm in diameter, sparsely pubescent to densely pubescent, hairs 0.3 mm long, appressed, light brown. Bracts 1, basal to sub basal, ca. 6 mm long and wide, length:width ratio ca. 1, very broadly ovate, apex acuminate, base truncate, pubescent outside, hairs ca. 0.2 mm long, appressed, light brown, glabrous inside. Flower buds up to 3 cm long, up to 1.5 cm in diameter, pyramidal, margins strongly refl exed. Sepals 1.5-2.5 cm long, 1-2 cm wide, length:width ratio 1.2-1.4, broadly ovate, tomentose brown, and sparsely pubescent inside, hairs 0.2 mm long, appressed, light brown; tomentose light brown outside, glabrous towards center. Sepals grey-green in fresh material, light brown to yellowish outside, yellowish inside along margins, black at center inside. Outer petals 2.5-4 cm long, 0.8-1.5 cm wide, length:width ratio 2-3, narrowly elliptic to elliptic, base narrowed, apex acute; densely pubescent outside, more so along central vein, hairs ca. 0.1 mm long, appressed, light brown; sparsely pubescent inside, hairs 0.1 mm long, appressed, light brown. Inner petals 1.5-2.8 cm long, 0.6-1.5 cm wide, length:width ratio 1.6-2.6, narrowly elliptic to elliptic, base narrowed, apex acute, pubescence similar to outer petals. Petals yellow to grayish-yellow in fresh material; dark brown to grey outside, black inside in herbarium material. Stamens 4-6 mm long, connective discoid, pubescent, ca. 1 mm in diameter, pinkish red. Carpels 5-10, 4-6 mm long, 1.5-2 mm in diameter, stigma weakly bilobed, ca. 2 mm in diameter, drying back, densely pubescent, hairs ca. 0.5 mm long, appressed upwards, light brown; ovules 24-35. Fruiting pedicels 1.5-5 cm long, 4-6 mm in diameter, woody, glabrous to sparsely pubescent. Monocarps 3-5, up to 9-10 cm long, 4-5 cm wide, globose to ellipsoid, generally straight; not ribbed, smooth, densely tomentose brown, light green in vivo, all over giving a velvety aspect; pale bluish green turning brown at maturity on fresh material; apex rounded, stipe 0-4 mm long, 3-5 mm wide; not rostrate. Seeds numerous per monocarp, 1.5-2.5 cm long, 1-1.5 cm wide, ellipsoid fl at, 5-9 mm in depth; testa black to brown, smooth, easily falling off revealing the ruminate endosperm; raphe raised; hilum 0.7-1 cm long, 3-5 mm wide, narrowly ellipsoid. Distribution. A widespread species across West and Central Africa. Found in Guinea, Liberia, Ivory Coast and Ghana, as well as in Nigeria, Cameroon, Gabon, Equatorial Guinea, Central African Republic, Republic of Congo and two specimens in Democratic Republic of Congo. Figure 11.
Habitat and ecology. Found in primary or secondary lowland rain forest. On tierra fi rme , or along rivers, occurring on sandy or rocky soils. Also found in gallery forests near savannas. 0-600m.
Phenology. Flowering and fruiting have been recorded across its distribution all year round.
Preliminary IUCN conservation status. LC. Th is species is the most widespread of all Uvariastrum species occurring in numerous national parks and other protected areas in both Central and West Africa, as well as being a common understory tree and is often collected. Th e Least Concerned category is recommended. Uses. Th e wood is hard and sometimes used for making guns in West Africa (Burkill 1985;Irvine 1961).
Notes. Uvariastrum pierreanum is characterized by a combination of light brown sepals and glabrous leaves. Th e leaves resemble those of U. germainii but the petioles are notably shorter and the apex shortly acuminate. Th e fruits are large smooth and pubescent with a green tinge when fresh in contrast to U. germainii that has smaller ribbed fruits.
Distribution. Th is species has a strict Central African distribution occurring from extreme east Nigeria and South East Cameron till Democratic Republic of Congo; 0-600 m. Figure 13.
Habitat and ecology. Occurring in primary or secondary lowland rain forest, on tierra fi rme with well drained soils, but also on marshy or sandy soils; 0-400 m.
Phenology. Flowering and fruiting all year round across its distribution range. Preliminary IUCN conservation status. LC. Th is species has a wide distribution across the Congo basin. It occurs in numerous national parks (Korup National Park (Cameroon); Loango National Park (Gabon) and other protected areas, and it is often collected. Th e least concern category is appropriate. Onana et al. (2005) gave the Near Th reatened (NT) status to U. zenkeri , but this was before U. pynaertii was sunken into synonymy and thus based on a smaller distribution. Uses. None recorded. Notes. Th is species is easily distinguished by the sepals that dry black and the large leaves with the leaf lamina inserted on top of the petiole. Th e black color of the dried sepals is related to the glabrous or sparsely pubescent outer side of the sepals, whereas it is pubescent in the other species.
Carpel number in this species appears very variable. Th e higher number of carpels compared to the other species ( U. zenkeri and U. pierreanum ) was one of the reasons why De Wildeman (1909) described the species U. pynaertii . I have counted the carpels for several specimens from DRC to Nigeria and there is a clear continuous variation from 1 to 15. Th e specimen with a single carpel is intriguing and has been described as a variety U. zenkei var. nigritanum (Talbot 1314). However, all other aspects of its morphology lead me to not accept it as distinct even at the rank of variety. What I can see is an increase in carpel number from Nigeria/Cameroon (3-5-10) to DRC (9-15), but this variation has yet to be properly explored. For these reasons I will keep this variation under a single species name.
Th e lectotype of U. zenkeri designated here followed the unpublished fl ora of Cameroon (Annonaceae) by Le Th omas (1969) that is archived at the Museum National d'Histoire Naturelle in Paris, kindly made available by Dr. Th ierry Deroin. Le Th omas selected Zenker 2935 as the lectotype over Zenker 2438 , the other syntype cited in the protologue. Because the former is more widely distributed I agree with her choice and select the B sheet designated here.
In the "Catalogue of the plants collected by Mr. and Mrs. P.A. Talbot" (Rendle et al. 1913) Baker indicates two collection numbers for var. nigritanum (pp 120): Talbot 3 and 1341 . Th e protologue clearly indicates that Talbot 1341 is the type. Of the 4 specimens I have located, the BM sheet has no indication of either the name or the collection number and with a 1911 date (indicated via a small stamp). Th e other sheets (FHO, K, P) all have the name, the collection number and the date (1912, see below). Th is leads me to suspect that the BM sheet is in fact Talbot 3 and thus isn't a type specimen. I here select the K! sheet as the holotype as this would have been seen by Baker (based in BM or K) and I do not consider the BM sheet as being a type specimen. LBV, LISC, M, MO, P, UPS, US, UC, WAG, and Z. Finally, I am grateful to two anonymous reviewers and Sandra Knapp for improving the manuscript thanks to their detailed comments on an earlier version. Access to ArcMAp 10.0 was provided via the IUCN Palm Specialist Group.