Discovery and conservation of Monanthotaxis bali (Annonaceae) a new Critically Endangered (possibly extinct) montane forest treelet from Bali Ngemba, North West Region, Cameroon

Monanthotaxis bali is the only known, solely montane (occurring solely above 2000 m alt.) species of the genus. It joins M. orophila (Rwanda) and M. discolor (Tanzania), two other species that can also occur above 2000 m alt. Monanthotaxis bali is an addition to the small number (28) of the tree species of the surviving montane forests of the Cameroon Highlands of which only eight other species are endemic. Due to its supra-axillary inflorescences, and petals arranged in one whorl but with the outer petals overlapping the inner petals distally, and rounded flower buds, the new species is placed in Monanthotaxis clade B of Hoekstra. The new species is unusual in having the largest outer petals in clade B, in being a treelet in a predominantly lianescent genus, and in lacking the glaucous underside of the leaf-blades that usually characterises the genus. Monanthotaxis bali takes the number of continental African species of the genus to 80, and makes Cameroon, with 30 species, the most species-diverse country for the genus. Monanthotaxis bali is known only from the Bali Ngemba Forest Reserve, a forest remnant under great pressure of degradation and clearance in the Bamenda Highlands of Cameroon. The case for protecting Bali Ngemba for its unique plant biodiversity is made. Monanthotaxis bali may already be extinct due to logging and agricultural activities. Here it is described, illustrated, mapped and assessed as Critically Endangered (Possibly Extinct) using the IUCN 2012 criteria.


Introduction
In January 2022, whilst examining herbarium specimens collected for the Conservation Checklist of the Plants of Bali-Ngemba, Cameroon (Harvey et al. 2004) but which had by oversight not been identified, an unknown taxon of Annonaceae was encountered. Darbyshire 375 was collected 11 April 2004 (K, YA) at 2110 m alt. This is an extremely high altitude for a member of Annonaceae to occur in the Cameroon Highlands. On the higher mountains, Mt Cameroon (4095 m alt) and Mt Oku (3011 m alt.), the highest recorded occurrences of Annonaceae are respectively at 1400 m (Uvariodendron fuscum (Benth.) R.E.Fr. and 1500 m alt. Monanthotaxis vulcanica P.H.Hoekstra (as M. littoralis (Bagsh. & Baker f.) Verdc. (Cable & Cheek 1998;Cheek et al. 2000). However, on Mt Kupe (2064 m), Xylopia africana (Benth.) Oliv. has been collected at 2050 m (Cheek 7065, Y, YA;Cheek et al. 2004: 241).
Darbyshire 375 was identified as a Monanthotaxis Baill. in the palaeotropical tribe Uvarieae, despite being a treelet with leaf-blades yellow-brown on the abaxial surface, when this genus is recognised by its lianescent habit and glaucous lower side of the leaves (Hoekstra et al. 2021). Pointers to placement in Monanthotaxis are the presence of a bract midway along the pedicel, the supra-axillary inflorescences and above all, the presence of dark coloured, gland-like structures at the base of the leaf blade, a feature almost exclusively present in Monanthotaxis and not found in other Annonaceae (Hoekstra et al. 2021). However, such gland-like structures are stated as being present in the Asian genera Desmos Lour. and Friesodielsia Steenis (anonymous reviewer, pers. comm.). Additional pointers to Monanthotaxis seen in Darbyshire 375 are the reduced number of stamens (nine), the separated anther thecae, and the long filaments, The Annonaceae is a pantropical family largely restricted to tropical rainforest habitats. The characteristic, often showy flowers and fruit help make it widely collected and studied (Chatrou et al. 2012;Couvreur et al. (2022)). Annonaceae are well known for species producing edible fruits (bullocks heart, soursop, custard apple), and for the fragrant ylangylang (Cananga odorata (Lam.) Hook.f. & Thomson) used in perfumes. The Annonaceae is a basal angiosperm family in the order Magnoliales (Heywood et al. 2007). It comprises c. 2400 species and c. 107 genera of trees, shrubs and lianas (Guo et al. 2017a). Within the subfamily Annonoideae comprising over 1500 species, the palaeotropical tribe Uvarieae is composed of 15 genera and 474 species (Guo et al. 2017a).
New Annonaceae taxa are continually being discovered in Africa, including new genera to science e.g. Lukea Cheek & Gosline in E Africa (Cheek et al. 2022d) and new species, e.g. of Uvariodendron (Dagallier et al. 2021) also in E Africa, and in Cameroon, new species such as Uvariopsis dicaprio Cheek & Gosline (Gosline et al. 2022), U. etugeana Dagallier & Couvreur (Couvreur et al. 2022) and Xylopia monticola D.M.Johnson & N.A.Murray (Johnson & Murray 2018) The genus Monanthotaxis is confined to subsaharan continental Africa (79 species), the Comores and Madagascar (Hoekstra et al. 2021). The numbers of species have been recently increased by the description of about 20 new species to science (Hoekstra et al. 2014(Hoekstra et al. , 2016(Hoekstra et al. , 2021 and the subsumation of Exellia Boutique and Gilbertiella Boutique, and the African species of the genera Friesodielsia Steenis (Guo et al. 2017b). Earlier, Verdcourt (1971 had subsumed the African species of Popowia Endl. and Enneastemon Exell into Monanthotaxis, recognising 55 species in the last genus. Monanthotaxis species are mainly confined to rainforest, with only a few species occurring in woodland, notably the widespread M. buchananii (Engl.) Verdc. In continental Africa species extend from Senegal in the north, and west to Somalia in the east, and as far south as the Eastern Cape Province of South Africa (Hoekstra et al. 2021).
Fifty four species occur in the Central African forest, with DR Congo and Cameroon both having the highest number of all countries: 29 species. Only a few forest species have wide distributions e.g. Monanthotaxis laurentii (De Wild.) Verdc. from Guinea in the west to eastern DR Congo in the east (Hoekstra et al. 2021). Hoekstra et al. (2021) identify nine different clades, A -I, based on 5 plastid and 2 nuclear DNA markers. Each clade is morphologically characterised. Seed dispersal is mainly recorded to be by primates including humans, gorillas, chimpanzees, mandrills and galagos in continental Africa, and in Madagascar, lemurs. The fruits are juicy, sweet and often brightly coloured red or orange (Hoekstra et al. 2021).
Several species are used in traditional medicine including as anti-malarials, and 15 species have been studied for their phytochemistry (Hoekstra et al. 2021).
The existence of a non-climbing species within a genus dominated by climbers is not unusual. Elsewhere in the Annonaceae, Uvaria chamae P.Beauv. is usually a shrub, when almost all other species of the genus are climbers. Additionally, liana species often begin life as shrubs, before becoming lianescent, however they are not usually reproductive in the shrubby stage as is the case in our taxon.

Materials and Methods
The specimen was collected using the patrol method as documented in Cheek & Cable (1997). Unambiguous identification as a new species was largely thanks to the excellent monograph including comprehensive species delimitations and keys, of Hoekstra et al. (2021) without which this paper would have been much more difficult to complete so speedily. Herbarium material was examined with a Leica Wild M8 dissecting binocular microscope fitted with an eyepiece graticule measuring in units of 0.025 mm at maximum magnification. The drawing was made with the same equipment with a Leica 308700 camera lucida attachment. Specimens, or their high-resolution images, were inspected from the following herbaria: BR, K, P and WAG. All specimens cited have been seen. The description of the new species is based on the examination of four duplicates of the type, including three rehydrated flowers. Names of species and authors follow the International Plant Names Index (IPNI continuously updated). Nomenclature follows Turland et al. (2018). Technical terms follow Beentje & Cheek (2003) and Hoekstra et al. (2021). The conservation assessment follows the IUCN (2012) categories and criteria. Herbarium codes follow Index Herbariorum (Thiers continuously updated).

Results
Because Darbyshire 375 has bisexual flowers, supra-axillary 1 -2-flowered inflorescences, 7 -9 carpels, 9 free stamens, no staminodes, inner petals visible between the outer petals in the rounded flower buds, hairy petals, ovules 4 -6, hairs on young branches yellow-brown, it keys out in Hoekstra et al. (2021) to couplet 45 which leads to Monanthotaxis barteri (Baill.) Verdc. of West Africa and M. schweinfurthii (Engl. & Diels) Verdc. (Central Africa). It differs from these two species in numerous characters (see Table 1  This group of species is characterised by rounded flower buds in which the inner petals are exposed between the bases of the outer petals. They also have a single whorl of both stamens (usually 9) and carpels (usually 6 -9), are supra-axillary (the inflorescences not arising immediately from the axil but some distance above it) and 1 -2-flowered. This group, Clade B, equates to the formerly accepted genus Enneastemon Exell. Within Clade B, Monanthotaxis bali is remarkable for having the largest petals of all species (see description below).
In the key to Monanthotaxis in the Flore du Cameroun account (Hoekstra in Couvreur et al. 2022), Darbyshire 375 keys out to couplet 21 due to its glabrous stems, leaf-blade length: breadth ratio 2 -3: 1, and supra-axillary inflorescences. However, it fills neither of the two statements at couplet 21 and in a future edition of this key the following couplet could be inserted at this point to accommodate the new species, and all subsequent couplets in the key renumbered by adding 1: 21. Treelet with leaves concolorous, occurring above 2000 m alt……… …………….M. bali 21. Lianas with leaves discolorous (glaucous abaxially), occurring below 2000 m alt…….22 Monanthotaxis foliosa and M. capea also occur in the Cameroon Highlands, the first reaching 1500 m, the second 1000 m elevation. Both also have rounded flower buds, 9 stamens and can have slightly supraaxillary infloresecences. The first differs in having adaxial leaf tertiary venation strongly raised; inflorescences normally 3 -16 flowered; sympodial rachis 3 -17 mm long; ovules 2 -3 (vs respectively, tertiary venation absent adaxially; inflorescences 1 -2-flowered, rachis absent, ovules 3 -4 in M. bali). Monanthotaxis capea differs in that the young branches are densely pubescent with ascending to erect reddishbrown hairs 0.2 -0.3 mm long, the petiole and abaxial blade also hairy (vs stem, petiole and abaxial blade glabrous) and the outer tepals of M. capea are 3.5 -5.0 × 2.0 -3.8 mm (vs 7.3 -7.6 × 7.1 -7.3 mm in M. bali).

RECOGNITION.
Monanthotaxis bali is similar to M. barteri and M. schweinfurthii in the bisexual flowers, 1 -2-flowered inflorescences, 7 -9 carpels, 9 free stamens, no staminodes, inner petals visible between the outer petals in the rounded flower buds, hairy petals, ovules 4 -6, hairs on young branches yellow-brown, It differs in being a treelet with concolorous leaves, supra-axillary inflorescences and flower buds 7 -9 mm diam. (vs lianas with blades glaucous below, axillary inflorescences and flower buds 2 -4.5 mm diam.). Additional diagnostic characters are given in Table 1 Although occurring within the Bali Ngemba Forest Reserve, Monanthotaxis bali is not protected because resources for patrolling seem so inadequate that people enter the forest to cut timber and plant food crops with impunity. Much of the montane, upper part of the reserve has been entirely cleared of forest for cultivation (Harvey et al. 2004), so it is fortunate that this single plant survived in one of the fragments that remained in 2004. Given continual pressure in the last 18 years it may be that this fragment has also been lost. Due to the ongoing Cameroon civil war (https:// en. wikip edia. org/ wiki/ Anglo phone_ Crisis accessed Nov. 2022) field visits to NW Region Cameroon have not been possible in the last five years.
This distinctive treelet has not been found in surveys elsewhere in the Cameroon HIghlands and adjacent areas (Cheek 1992;Cheek et al. 1996;Cable & Cheek 1998;Cheek et al. 2000;Maisels et al. 2000;Chapman & Chapman 2001;Cheek et al. 2004;Harvey et al. 2004;Cheek et al. 2006Cheek et al. , 2010Harvey et al. 2010;Cheek et al. 2011). Therefore, it may be, or have been, endemic to Bali Ngemba. Several other plants of high altitudes in the Cameroon Highlands appear to be point endemics e.g. Impatiens etindensis Cheek & Eb.Fisch. (Balsaminaceae, Cheek & Fischer 1999), Ledermanniella pollardiana Cheek (Podostemaceae, Cheek & Ameka 2008) and Kupeantha fosimondi (Cheek) Cheek (Rubiaceae), Cheek et al. 2018a). However, others, originally thought to have been point endemics have since been found at one or more other locations in the highlands of Cameroon, e.g. Coffea montekupensis Stoffelen (Rubiaceae, Stoffelen et al. 1997) and Impatiens frithii Cheek (Balsaminaceae, Cheek & Csiba 2002). It is to be hoped that the second scenario will be the case for Monanthotaxis bali and that it will also be found at other locations, although we consider this unlikely.
Bali Ngemba is less than 8 km 2 in area, and it was relatively well-surveyed by large teams of botanical collectors (Harvey et al. 2004). Other new, or rediscovered species from Bali-Ngemba are known from multiple gatherings, sometimes 10 or more e.g. Leptonychia kamerunensis Engl. & K.Krause (Byttneriaceae, Cheek et al. 2013), Vepris onanae Cheek (Cheek et al. 2022a). That only a single collection is known for Monanthotaxis bali, and that a single plant was reported (Darbyshire 375) suggests that the species is genuinely infrequent, if indeed it survives.
Here we assess Monathotaxis bali as Critically Endangered (Possibly Extinct), CR (PE) B1+B2ab(iii) +D since only a single individual was reported from a forest scrap, threats are ongoing, and AOO estimated as 4 km 2 using the cells of that size preferred by IUCN, while EOO is estimated as <5 km 2 using IUCN (2012) guidance. It has been estimated that 96.5% of the former area of the montane and submontane forests of the Bamenda Highlands has been lost to clearance (Cheek et al. 2000). The surviving forests of the Bamenda Highlands are extremely fragmented. The indications for seed dispersal in Monanthotaxis are that it is conducted by fruit-eating primates (e.g. chimpanzees) (Hoekstra et al. 2021) for which traversal of human-created habitat (farmland and secondary grassland) in the Cameroon Highlands is known to be problematic (Cheek et al. 2021a).  Harvey et al. 2004). Newly described Endangered, tree species from Bali Ngemba include Tricalysia elmar Cheek (Rubiaceae, Cheek et al. 2020a), Vepris onanae Cheek (Cheek et al. 2022a) and Deinbollia onanae Cheek (Cheek et al. 2021a).
Sadly, Monanthotaxis bali is not the only seemingly point endemic in the genus in Africa. Eight other species are known from a single collection or location: Monanthotaxis aquila P.H.Hoekstra (DR Congo, last seen >100 years ago) and M. zenkeri P.H.Hoekstra (Bipinde, Cameroon, last seen 100 years ago). All of these species, completely logically, are treated as Critically Endangered by Hoekstra et al. (2021).
Monanthotaxis bali of Cameroon occurs within the Cross-Sanaga Interval (Cheek et al. 2001) which has the highest species and generic diversity per degree square in tropical Africa (Barthlott et al. 1996;Dagallier et al. 2020) including endemic genera such as Medusandra Brenan (Peridiscaceae, Breteler et al. 2015;Soltis et al. 2007). Much of this diversity is associated with the Cameroon Highland areas, different highlands each having a species of a genus e.g. as in Kupeantha Cheek (Rubiaceae, Cheek et al. 2018a). However, unlike for many genera in Africa, such as Vepris (Cheek et al. 2022a) and Impatiens (Cheek et al. 2022b), the Cross-Sanaga is not notable as a centre of diversity for the genus Monanthotaxis, since it holds only 14 species of the genus, of which three are endemic to the interval, increasing to four with the publication of Monanthotaxis bali.
In tropical Africa Annonaceae predominantly occur in lowland evergreen forest. A remarkable feature of Monanthotaxis is that 33 of the 79 species documented by Hoekstra et al. (2021) can occur over 1000 m alt., while four other species occur only above 1000 m alt, two others occurring sometimes above 2000 m (see introduction).

Discussion and Conclusions
Monanthotaxis bali joins the growing list of African species considered likely to be extinct. Species considered extinct in Cameroon are Oxygyne triandra Schltr., Afrothismia pachyantha Schltr. (Cheek & Williams 1999;Cheek et al. 2018cCheek et al. , 2019a. It seems possible that Monanthotaxis bali became extinct before it is formerly named scientifically in this paper, as was the case with Vepris bali, also of higher altitudes in Bali Ngemba (Cheek et al. 2018b). This extinction crisis extends through W Africa e.g. Saxicolella deniseae Cheek, also seemingly extinct before publication (Cheek et al. 2022c). Similarly, Pseudohydrosme bogneri Cheek & Moxon-Holt and P. buettneri Engl. are now considered extinct in neighbouring Gabon (Moxon-Holt & Cheek 2020;Cheek et al. 2021b).
About 2000 species of vascular plant have been described as new to science each year for the last fifteen years or more. Cameroon currently has the highest number of new species to science published each year (Cheek et al. 2020b), recent examples being published are (Achoundong et al. 2021;Alvarez-Aguirre et al. 2021;Cheek et al. 2021a, b, c;Cheek & Onana 2021;Couvreur et al. 2022;Gosline et al. 2022). While some exceptions exist (Cheek & Etuge 2009;Cheek et al. 2019b), many, probably most of these species are highly range-restricted, making them especially at risk of habitat destruction, and so likely to be rated as threatened when assessed.
Only 7.2% of the 369,000 flowering plant species (the number is disputed) known to science have been assessed on the IUCN Red List. (Bachman et al. 2019;Nic Lughadha et al. 2016. Thanks to the Global Tree Assessment (BGCI 2021) many of the world's tree species have now been assessed. The State of the World's Trees concluded that the highest proportion of threatened tree species is found in Tropical Africa, and that Cameroon has the highest number (414) of threatened tree species of all tropical African countries (BGCI 2021). This will be further increased by the addition of Monanthotaxis bali and will require the updating of the Red Data Book of Cameroon Plants (Onana & Cheek 2011). However, the vast majority of plant species still lack assessments on the Red List (Nic Lughadha et al. 2020).
It is imperative to uncover the existence of previously unknown species as soon as possible and to formally name them. Until this is done, they are invisible to science and the possibility of them being assessed for their conservation status and appearing on the IUCN Red List is greatly reduced (Cheek et al. 2020b), limiting the likelihood both that they will be proposed for conservation measures, and that such measures will be accepted.
Bali Ngemba, while a Forest Reserve, is not formally protected for nature conservation and its natural forest habitat is being encroached for agriculture. Protection of Bali Ngemba, with the support of local communities supported by designation as a TIPA (Darbyshire et al. 2017) is essential if the 12 endemic and near-endemic plant species unique (or nearly unique) such as Monanthotaxis bali are not to become extinct globally, and if the 34 threatened species of that forest are not to move closer to extinction.

Acknowledgements
This paper was completed as part of the Cameroon TIPAs (Tropical Important Plant Areas) project at RBG, Kew, which is supported by Players of Peoples Postcode Lottery. We thank Lydia Burns and Penny Applebe of Kew's Foundation for making this possible. The specimen cited in this paper was collected with the support of volunteers arranged by Earthwatch Europe, Oxford, and we were also assisted greatly by colleagues in Cameroon such as the late Martin Etuge, Innocent Wultoff and Terence Atem. John DeMarco of the then Bamenda Highlands Forest Project persuaded us to make a botanical survey of Bali Ngemba forest in the Bamenda Highlands, and with Anne Gardner supported our visits. The late Dr Benoît Satabié, Drs Gaston Achoundong, Florence Ngo Ngwe, Eric Nana, Jean Lagarde Betti, the current and former leaders, of IRAD-National Herbarium of Cameroon, Yaoundé, and their staff are thanked for expediting the collaboration between our two institutes. Janis Shillito typed the manuscript. Thomas Couvreur and an anonymous reviewer are thanked for constructively reviewing an earlier version of this paper.

Conflict of interest
The authors declare that they have no conflict of interest.
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