Three new species of Uvariodendron (Annonaceae) from coastal East Africa in Kenya and Tanzania

Abstract East Africa is a hotspot of biodiversity with many endemic plant species. We describe three new species of the genus Uvariodendron (Annonaceae) from the coastal forests of Kenya and Tanzania. Uvariodendron mbagoi Dagallier & Couvreur, sp. nov. is endemic to Tanzania and unique within the genus by its strong bergamot scent and its tomentose fruits having regular tufts of higher hair density. Uvariodendron dzomboense Dagallier, W.R.Q. Luke & Couvreur, sp. nov. is endemic to Dzombo Hill in Kenya and is rendered distinct by its small leaves and very densely pubescent carpels. Uvariodendron schmidtii W.R.Q. Luke, Dagallier & Couvreur, sp. nov. is endemic to Shimba Hills in Kenya and differs by its small flowers and fused sepals forming a ring. Following IUCN criteria we assessed U. mbagoi and U. dzomboense as endangered (EN) while U. schmidtii is assessed as Vulnerable (VU). We also propose a new combination: Polyceratocarpus oligocarpus (Verdc.) Dagallier, comb. nov. The description of these three new species underlines the richness in endemics in East Africa and that new discoveries might arise from further botanical exploration of this region.


Introduction
East Africa is one of the richest regions in terms of biodiversity across the continent (Myers et al. 2000;Linder 2001). Recently, this region has been described as acting both as a "cradle" (i.e. promoting lineage divergence) and as a "museum" of diversity (i.e. maintaining old lineages), due to its topographical heterogeneity (Dagallier et al. 2020). East Africa harbors an incredible number of endemic species, particularly in the Eastern Arc Mountains and in coastal forests (Burgess et al. 1998(Burgess et al. , 2007Küper et al. 2004). Despite the completion of the Flora of East Africa series (Beentje 2015), East Africa still needs further botanical exploration . Indeed, from animals (Huber and Warui 2012) to plants (Poulsen and Lock 1997;Friis et al. 2015), new taxa continue to be described.
Annonaceae is a pantropical family of trees, shrubs and lianas. It is the most species rich family within the order Magnoliales, with ca. 2400 recognized species (Chatrou et al. 2012). In East Africa, several new species have been described for the region following the publication of the Flora of Tropical East Africa (Vollesen 1980;Verdcourt and Mwasumbi 1988;Johnson et al. 1999;Deroin and W.R.Q. Luke 2005;Couvreur et al. 2006;Couvreur and W.R.Q. Luke 2010;Marshall et al. 2016;Johnson et al. 2017;Gosline et al. 2019).
The genus Uvariodendron contains a total of 14 species restricted to tropical Africa (Fries 1930;Le Thomas 1967, 1969Verdcourt 1969Verdcourt , 1986. It belongs to the Monodoreae tribe (Chatrou et al. 2012) and was inferred to be the sister genus to the Uvariopsis -Monocyclanthus clade based on molecular data (Couvreur et al. 2008;Guo et al. 2017). Like many Annonaceae species, Uvariodendron species are trees with simple hair indumentum and palgiotropic branches on an orthotropic axis. Their leaves are distichous, simple and entire, with the midrib sunken above, raised below, the secondary veins weakly brochidodromous to brochidodromous and the tertiary veins reticulate. They have hermaphroditic flowers with one whorl of three valvate to imbricate sepals and two whorls of three free and valvate petals. Uvariodendron species don't have a single synapomorphy that can differentiate them from other Annonaceae at first sight, but they can be recognized by the combination of the several characters presented hereafter. The inflorescence is axillary or on the trunk, composed of one to three sessile flowers or with a short pedicel (generally less than 5 cm). The sepals are smaller than, and morphologically different to, the petals. The outer and inner petals are subequal in length, from 10 to 40 mm at anthesis; the outer petals are valvate all along the margin whereas inner petals are valvate only at the apex. The stamens are numerous (more than 200), with linear anthers and truncate connective. The carpels are free, linear, with a coiled stigma. The monocarps are sessile or subsessile and cylindrical.
Here we describe three new species of Uvariodendron, from coastal forests in Kenya and Tanzania. We also transfer the species known as Uvariodendron oligocarpum Verdc. within the genus Polyceratocarpus Engl. & Diels as Polyceratocarpus oligocarpus (Verdc.) Dagallier. This brings the number of Uvariodendron species up to nine for East-Africa, and 17 for the genus as a whole. A key to East-African Uvariodendron species is also presented.

Material and methods
We examined all the 35 herbarium specimens cited in the results. Among them, we measured 12 specimens for Uvariodendron mbagoi (three of which were also examined and measured as living individuals), three herbarium specimens for Uvariodendron dzomboense, and four herbarium specimens for Uvariodendron schmidtii. Herbarium specimens came from B, DSM, EA, K, MPU, MO, P, and WAG. The three new species are morphologically close to Uvariodendron kirkii Verdc., one of the other Uvariodendron species occurring in East Africa. In order to ease the discrimination between the species, we present a comparison table of the most discriminant characters between the four species (Table 1). The data for Uvariodendron kirkii is taken from Verdcourt (1971) and from more than 50 specimens examined in the above-mentioned herbaria.
For morphological descriptions, we followed the terminology developed by Hickey et al. (1999) and by the Systematics Association Committee for Descriptive Biological Terminology (1962) for leaf and plane shapes, by Payne (1978) for the indumentum, and by Harris and Harris (2001) for the other terms.
To make a preliminary conservation status assessment for each species, we calculated the extent of occurrence (EOO) and the area of occupancy (AOO) using the ConR package . When calculation of EOO and AOO was impossible due to imprecision of coordinates, as for Uvariodendron dzomboense and for Uvariodendron schmidtii, we calculated the area of the locality in which they occur (respectively the forested part of Dzombo Hill and the Longomwagandi forest) based on Google satellite images with the surface calculation tool in QGIS v. 2.18.17 (QGIS Development Team 2016). We then assigned a preliminary conservation status following IUCN Red List Categories and Criteria Version 3.1 (IUCN 2012).
The distribution map was plotted using ggmap (https://CRAN.R-project.org/ package=ggmap) package in R (R Core Team 2016). Data on protected areas was taken from Protected Planet (https://www.protectedplanet.net/, accessed June 2018). Diagnosis. Differs from other Uvariodendron species by its stiff greyish-green leaves with slightly revolute margins, the strong bergamot scent (the citrusy smell of Citrus bergamia Risso, between lemon and orange scent) of crushed leaves and bark, its globose flower buds easily falling off and its tomentose fruits having regular tufts of higher hair density. Differs from Uvariodendron kirkii by having smaller leaves when looking at the greater leaves (157 mm maximum vs. 210 mm maximum) ( Table 1).
Conservation status. This species is known from 11 records in seven locations. The current occurrence of the species in Mkulumuzi river and Hale is really unlikely given that these are now (sub)urban areas and that these records date back, respectively, more than 30 years and over a century. Changes in traditional practices and exploitation of traditionally protected forests had been observed more than 20 years ago (Mwihomeke et al. 1998). This indicates that the current occurrence of the species in Kwedivikilo sacred forest is uncertain. Kwedijela forest is a locality under deforestation pressure with local crops slowly gaining ground (L-P.M.J. Dagallier and F. Mbago, field observations). However, the occurrences of the species in Kwedijela forest are 500 meters from the limit of Saadani National Park (SNP), so the species is likely to occur within the SNP where the protection is strict. The only record of this species occurring within a protected area is in Kimboza Forest Reserve, which has been threatened by encroachment, logging and invasion by the exotic Cedrela odorata L. (Hall andRodgers 1986, Patrick 2008).
For the reasons explained above, we removed the occurrences in Mkulumuzi river and Hale from the calculations of extent of occurrence (EOO) and the area of occupancy (AOO). Considering the five remaining localities, the EOO is 3867 km 2 and AOO is 20 km 2 . Following IUCN criterion B (IUCN 2012), Uvariodendron mbagoi is therefore assigned a preliminary status of Endangered EN B1ab(i,ii,iii,iv)+2ab(i,ii,iii,iv). Uses. The bark is used as a spice for meat meals and for tea. Additional field notes. Foodplant of Graphium kirbyi (Papilionidae) (T.C.E. Congdon 532).
Etymology. Named after Mr. Frank Mbago, curator of the Dar es-Salaam University herbarium (DSM), to whom we owe the discovery of this species, and in honor of his botanic knowledge and fieldwork expertise in Tanzania, in particular of Annonaceae. He is also co-discoverer of the endemic Tanzanian genus Mwasumbia ).
Paratypes. Tanzania  Discussion. Uvariodendron mbagoi is unique within Uvariodendron for the strong bergamot (Citrus bergamia Risso) scent of the crushed leaves and bark. This scent is between lemon and orange scent. Other African Annonaceae species present strong scents. For example, Uvariodendron anisatum Verdcourt (Verdcourt 1955) presents an aniseed scent, and Uvariodendron molundense (Diels) R.E.Fries var. citrata Le Thomas (Le Thomas 1969) and Uvariopsis citrata Couvreur & Niangadouma (Couvreur and Niangadouma 2016), present a lemon scent. However, no bergamot scent has been reported so far in Annonaceae.
The globose flower buds of this species easily fall off. Only flower buds were observed for this species, thus it is hard to infer the size of mature flowers. In the description above, the measures on the sepals and the petals are based on the dissection of the biggest flower bud of U. Bloesch s.n., and the carpel measurements were based on an old flower of T.C.E. Congdon 532 which has lost sepals and petals.
The fruiting specimens observed were collected from September to December. Collecting this species earlier in the year might permit the observation of flowers at anthesis. Diagnosis. This species differs from other Uvariodendron species by its 50-75 carpels that are densely pubescent and its leaves smaller than 150 mm in length and narrowly elliptic to elliptic. It differs from U. kirkii by its smaller leaves (132 mm maximum versus 210 mm maximum) and higher number of carpels (50-75 versus 7-20) (Table 1).
Habitat. Moist semi-deciduous forest on igneous intrusion. Conservation status. This species is known from five collections from a single location. Literature found on the Dzombo Hill forest reports a surface of 2.95 km 2 (Critical Ecosystem Partnership Fund 2005). We calculated a surface of 5.31 km 2 for the forested part of the hill (see Material and Methods for details). EOO and AOO are thus estimated at less than 5.40 km 2 . The Kaya Dzombo forest is gazetted as a sacred forest under the National Museums protection as a National Monument. However, the forest suffers from local logging for timber, poles and firewood, and has been impacted by fire on several occasions (W.R.Q. Luke, personal observations). Following IUCN criterion B (IUCN 2012), Uvariodendron dzomboense is therefore assigned a preliminary status of Endangered EN B1ab(iii)+2ab(iii).
Etymology. The specific epithet comes from the Dzombo Hill where the species is endemic.
Paratypes Discussion. This species is known as "Uvariodendron sp. nov. 1 of CFS" in the annotated checklist of the coastal forests of Kenya (Ngumbau et al. 2020).
The only fruit known from this species (Robertson S.A. et al. MDE 207) presents ca. 35 ovoid monocarps. These are densely pubescent and have small seeds compared to other Uvariodendron species (4.5 mm long vs. 8-20 mm long). However, it is unclear whether this observed fruit is ripe or not. Further collections could bring more information. This species also presents an 'eragrostiform' leaf-bud (see discussion of Uvariodendron schmidtii below).
During a field trip in Tanzania in November 2019, we explored the forest of Kilulu hill (TANZANIA-Tanga, 4°46'22"S, 39°07'30"E, see Fig. 2). Kilulu hill is ca. 40 kilometers as the crow flies south from Dzombo hill were U. dzomboense occurs. We expected to find U. dzomboense there but our quest on every slope of the hill was unsuccessful. This indicates that the dispersal distance of U. dzomboense might be very short. Diagnosis. This species differs from other Uvariodendron species by its flowers that are small (petals < 13 mm long), velutinous, on a 10-15 mm long pedicel, with fused sepals forming a ring around the fruit pedicel, and fewer than 10 carpels. It differs from U. kirkii by its smaller petals (< 13 mm versus more than 15 mm) and its sepals fused in a ring (versus free and valvate to imbricate) (Table 1).
Distribution. Endemic to Kenya; only known from the Longomwagandi forest (also found spelled "Longomagandi" or "Longo-Magandi" in the literature) in the Shimba Hills National Reserve, in Kenya (Fig. 2).
Conservation status. This species is known from seven collections from a single location. Literature for the Shimba Hills forest reserve reports a surface between 0.22 km 2 (Schmidt 1992) and 1.50 km 2 (Cheek 2003) for Longomwagandi forest. We calculated a surface of 1.30 km 2 (see Material and methods for details). EOO and AOO are thus estimated at less than 1.50 km 2 . Following IUCN criterion B, this would place the species in the "Critically Endangered CR" category. However, given that the occurrences are in the Shimba Hills National Reserve, no decline is observed or projected in EOO and AOO. The future of Uvariodendron schmidtii relies on the future of Shimba Hills National Reserve. Given that the species occurs in a single locality with a very restricted AOO (less than 20 km 2 ), it is "prone to the effects of human activities or stochastic events within a very short time period in an uncertain future, and is thus capable of becoming Critically Endangered or even Extinct in a very short time period" (IUCN 2012). Following IUCN criterion D, it can be therefore assigned a preliminary status of Vulnerable VU.
Copious seedlings are found below parent trees, but few survive to maturity. Many of these "wildlings" were moved to the Base Titanium indigenous tree nursery and have been out-planted there as part of their mine rehabilitation program. Vernacular name. Mbebeneka in Kidigo language (R. Schmidt 788).
Etymology. This species is named after Robert Schmidt, a PhD student studying the ecology of the Shimba Hills National Reserve who first collected it in September 1988 and brought it to the attention of W.R.Q. Luke.
Paratypes Discussion. This species shows 'eragrostiform' leaf-buds, a feature described in Uvariodendron gorgonis Verdcourt (Verdcourt 1969) and Uvariodendron dzomboense Dagallier, W.R.Q. Luke & Couvreur (this publication). This structure is composed of several (5-7 in U. schmidtii and U. dzomboense, 6-12 in U. gorgonis) distichous and densely pubescent scales that might be a protection for the apical meristem against drought or herbivores. The adjective 'eragrostiform' refers to the genus Eragrostis (Poaceae) that has a peculiar form of flattened spikelet composed of compact and clustered florets. Even though this feature is striking, it seems hard to use it as a diagnostic character. Similar apical buds are also found in other Annonaceae species such as Monodora minor Engler & Diels (Couvreur 2009)  We examined 11 specimens (including the type specimen) of Uvariodendron oligocarpum Verdc. and found they have percurrent tertiary venation and pitted seeds. These characteristics are typical of the genus Polyceratocarpus Engl. & Diels . Moreover, the fertile specimens observed have the combination of the following characters: outer petals ca. 35 mm long, 3 to 6 carpels, and 2 to 4 cylindrical and straight to slightly curved monocarps. This combination precludes these specimens from being identified as one of the two other species known from East Africa to date: Polyceratocarpus scheffleri Engl. & Diels that has "at least 20 [and] strongly curved" monocarps (Verdcourt 1971), and Polyceratocarpus askhambryan-iringae A.R. Marshall & D.M. Johnson that has outer petals 10-16 mm long (Marshall et al. 2016). Based on the above characters, they also cannot be included in any other accepted species from Central or West Africa that all have petals shorter than 25 mm long: Polyceratocarpus angustifolius Paiva and P. germanii Boutique, P. gossweileri (Excell) Paiva, P. laurifolius Paiva, P. microtrichus (Engl. & Diels) Ghesq. ex Pellegr., P. parviflorus Ghesq., and P. pellegrinii Le Thomas (Pellegrin 1949, Boutique 1951, Le Thomas 1965, Paiva 1966 (Burgess et al. 1998(Burgess et al. , 2007, and single-location endemic species are known there (e.g. Scharff 1992, Couvreur et al. 2009, Gosline et al. 2019. The discovery of these three new narrowly endemic species supports this long-standing observation. This also shows that botanically this region is still not fully known despite the publication of the complete flora of East Africa (Beentje 2015). There are still new plant species that have been collected and await description (see e.g. "sp. nov." for several genera in Ngumbau et al. 2020).
The new combination and the three new species described here bring the number of East African Uvariodendron species to nine across East Africa, and to 17 across Africa. The described species show characters that have never been found in the family, such as the strong bergamot scent of Uvariodendron mbagoi or in the genus, such as the very densely pubescent carpels and monocarps of U. dzomboense.