$¢PhytoKeys
PhytoKeys 233: 1-200 (2023) DOI: 10.3897/phytokeys.233.103096
Monograph
Phylogenomic inference of the African tribe Monodoreae (Annonaceae) and taxonomic revision of Dennettia, Uvariodendron and Uvariopsis
Léo-Paul M. J. Dagallier’?®, Frank M. Mbago?, Marie Couderc’®, Myriam Gaudeul‘, Aurélie Grall>©®, Caroline Loup’, Jan J. Wieringa®®, Bonaventure Sonké®®, Thomas L. P. Couvreur'®
er wo ND —
05, France
eo ON D
Yaoundée, Cameroon
DIADE, Université de Montpellier, IRD, CIRAD, Montpellier, France
Institute of Systematic Botany, The New York Botanical Garden, Bronx, New York 10458, USA
The Herbarium, Botany Department, Box 35060, University of Dar es Salaam, Dar es Salaam, Tanzania
Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle-CNRS-SU-EPHE-UA, 57 rue Cuvier, CP 39, 75231 Paris, Cedex
Herbaria Basel, Department of Environmental Sciences, University of Basel, Basel, Switzerland
Herbarium, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK
Herbier MPU, DCSPH - CC 99010, Université de Montpellier, 163 rue A. Broussonnet, F-34090 Montpellier, France
Naturalis Biodiversity Center, Darwinweg 2, 2333 CR, Leiden, Netherlands
Laboratoire de Botanique systématique et d'Ecologie, Département des Sciences Biologiques, Ecole Normale Supérieure, Université de Yaoundé |, BP 047,
Corresponding author: Léo-Paul M. J. Dagallier (leopauldagallier@gmail.com)
OPEN Qaceess
Academic editor: A. E. Ortiz-Rodriguez Received: 7 March 2023
Accepted: 16 August 2023
Published: 22 September 2023
Citation: Dagallier L-PMJ, Mbago FM, Couderc M, Gaudeul M, Grall A, Loup C, Wieringa JJ, Sonke B, Couvreur TLP (2023) Phylogenomic inference of the African tribe Monodoreae (Annonaceae) and taxonomic revision of Dennettia, Uvariodendron and Uvariopsis. PhytoKeys 233: 1-200. https://doi.org/10.3897/ phytokeys.233.103096
Copyright: © Léo-Paul M. J. Dagallier et al. This is an open access article distributed under terms of the Creative Commons Attribution License (Attribution 4.0 International -
CG BY 4:0):
Abstract
Monodoreae (Annonaceae) is a tribe composed of 11 genera and 90 species restricted to the tropical African rain forests. All the genera are taxonomically well circumscribed except the species rich genera Uvariodendron and Uvariopsis which lack a recent tax- onomic revision. Here, we used a robust phylogenomic approach, including all the 90 currently accepted species, with several specimens per species, and based on more than 300 Annonaceae-specific nuclear genes, to infer the phylogenetic tree of the Mono- doreae and test the limits between the genera and species. We recover all the genera as monophyletic, except the genus Uvariopsis for which the species Uvariopsis tripetala falls outside this clade. We thus reinstate the monotypic genus Dennettia for its single species Dennettia tripetala. We also erect a new tribe, Ophrypetaleae trib. nov., to ac- commodate the genera Ophrypetalum and Sanrafaelia, as we recover them excluded from the Monodoreae tribe with good support. Below the genus level, the genera /s- olona, Monodora, Uvariastrum, Uvariodendron and Uvariopsis show weakly supported nodes and phylogenetic conflicts, suggesting that population level processes of evo- lution might occur in these clades. Our results also support, at the molecular level, the description of several new species of Uvariodendron and Uvariopsis, as well as several new synonymies. Finally, we present a taxonomic revision of the genera Dennettia, Uvari- odendron and Uvariopsis, which contain one, 18 and 17 species respectively. We provide a key to the 11 genera of the Monodoraeae and describe four new species to science: Uvariodendron kimbozaense Dagallier & Couvreur, sp. nov., Uvariodendron mossambi- cense Robson ex Dagallier & Couvreur, sp. nov., Uvariodendron pilosicarpum Dagallier & Couvreur, sp. nov. and Uvariopsis oligocarpa Dagallier & Couvreur, sp. nov., and pro- vide provisional descriptions of three putatively new species. We also present lecto- typifications and nomenclatural changes implying synonymies and new combinations
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
(Uvariodendron citriodorum (Le Thomas) Dagallier & Couvreur, comb. et stat. nov., Uvari- odendron fuscum var. magnificum (Verdc.) Dagallier & Couvreur, comb. et stat. nov., Uvariopsis congensis var. angustifolia Dagallier & Couvreur, var. nov., Uvariopsis guineen- sis var. globiflora (Keay) Dagallier & Couvreur, comb. et stat. nov., and Uvariopsis solhei- dii var. letestui (Pellegr.) Dagallier & Couvreur, comb. et stat. nov.).
Résumé
La tribu des Monodoreae (Annonaceae) est composée de 11 genres et 90 espéces des foréts tropicales humides d'Afrique. Tout les genres sont taxonomiquement bien resolus, a part les genres Uvariodendron et Uvariopsis qui manquent d'une révision taxonomique récente. Ici, nous avons utilisé une approche phylogénomique robuste pour estimer l’arbre phylogenetique des Monodoreae, et tester les limites de genres et d’especes. Pour cela, nous avons inclut les 90 especes acceptées, et avons séquence plus de 300 genes. Tous les genres sont retrouves monophyletiques, a part le genre Uvariopsis pour lequel l'’espéce Uvariopsis tripetala se retrouve exclue. Nous rétablis- sons donc le genre monotypique Dennettia et son unique espéce Dennettia tripetala. Nous érigeons une nouvelle tribu, les Ophrypetaleae trib. nov., pour accueillir les genres Ophrypetalum et Sanrafaelia, car nous les retrouvons exclus de la tribu des Monodoreae avec un bon support. Au niveau infra-générique, les genres /solona, Monodora, Uva- riastrum, Uvariodendron et Uvariopsis montrent de faibles supports de noeuds et des conflits phylogénétiques, ce qui Suggére que des processus d’évolution se déroulent au niveau des populations. Nos résultats soutiennent également, sur un plan moléculaire, la description de plusieurs nouvelles especes d’Uvariodendron et d’Uvariopsis, de méme que plusieurs synonymies. Enfin, nous présentons une révision taxonomique des genres Dennettia, Uvariodendron et Uvariopsis, qui contiennent respectivement un, 18 et 17 es- peces. Nous fournissons une clé des 11 genres de Monodoreae, et décrivons quatre nouvelles espéces pour la science: Uvariodendron kimbozaense Dagallier & Couvreur, sp. nov., Uvariodendron mossambicense Robson ex Dagallier & Couvreur, sp. nov., Uva- riodendron pilosicarpum Dagallier & Couvreur, sp. nov. et Uvariopsis oligocarpa Dagallier & Couvreur, sp. nov., et fournissons une description provisoire de trois autres poten- tielles. Nous effectuons des lectotypifications et des changements nomenclaturaux tels que des synonymies et des nouvelles combinaisons (Uvariodendron citriodorum (Le Thomas) Dagallier & Couvreur, comb. et stat. nov., Uvariodendron fuscum var. magnifi- cum (Verdc.) Dagallier & Couvreur, comb. et stat. nov., Uvariopsis congensis var. angusti- folia Dagallier & Couvreur, var. nov., Uvariopsis guineensis var. globiflora (Keay) Dagallier & Couvreur, comb. stat. nov., et Uvariopsis solheidii var. letestui (Pellegr.) Dagallier & Couvreur, comb. stat. nov.).
Key words: conservation, evolution, new species, phylogeny, tropical rain forests
Table of contents
NGROGCICTION I. ekki ie Bn Ie ESN 2 ke OS A Ga 7 eS a 5 MaLerialSarichMel nO Gs -nccrcescctenectneddccemuevtets ety rx Faro aecuae ap tvaceteuninceneiy ies accbenmsitenes 7 TaxXQnmomMuUCieMISIONes. 2. .cchs Sei S0 ees 08e Sake Re. ain ly LN es So ee, Sad, vA PBR VIOG CROWES ql RB cians ree Memamnareie erates Ta aie kena ten ocd ree 8 Lesh <oinecyelag) oll ia(e Vakprene See Moe erp ei i Pe es, SOE EO RRSA E 8 DNA extraction, library preparation and SE€QUENCING................ccscceceesseeeeeneees 8 RaWwisequencebiOinfOrimatl GS oc ..9)....cecigi0 a eencotglsstng as Besshendddcaemaonieespodes 9 Gontigrassembly-and alignment. isiu. tte ance A eda lvlei 9
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 2
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
PRYIOGENETE TSC ONSTCUGH OM: ccc. de cmsrnapcemaenceuswesappbecumsnactussunnenteconesedamueuec peed 9 COMCALEM ATOM ADIORO AG Nx gaz sash ated htedn sate R ta caai teeta cnette wandonndtindes.notbieneedetes 9 GENE Trees EPPO GCE as Ae Sh. lente otal: cayenne LaRE een oe. lh 10 POS UES ret ars wcsese Crest nee tae chet Nara adore as peti ce AG tease eet. ee geen! 10 SPSCIMETIS-CX SMC Clea cre cere ester h eer ee rest et Tae aecucns cies etme eee Moores? 10 Pavel OG CR GHNNG S24, ed. bea Scores de Re neat hae ek be Sy Be renee Meth carte, Bay Pee A de 10 PROG SNe Tere LOM SIND Secsye ect lien tle tats Ae me oht fed es Meets ee ee eel ie 10 DISCUSSION xy. ceveccattaaes ides uocshs ceakeeanuQeniuee ndgeatrors cx dns caueacvaaauviceie weap seaatetayu ease accacocmeu’ 14 Phylogenomics of the Monodoreae tribe..............ccccecsccccsseceessceesececsteeeeseeeeees 14 RE-GIPCUMSERIPHOMUOT TNEMMDE: eens hE eK oh oe etre al ean ae teeta 15 PAST OT ORT specceeccsarctes cau ceeeeasusseeei ange cose tiniees tea spo taceise bee aa meg PhS Rane hae pe bse see oee 17 [if 2) 02 11010) BS bank cise pe Sree pant eon enh rte pt a orrah ch A De bret ot 12 OV FTA SUNY Sere x teresa etate coNopecacrchas at oddee ire trak tates lt cemcmace ad epetee dh «deanna des Nessemaace 18 The case of the newly described Genus LUKCA..........cecccceceesecessceesseeeeseeeesees 18 DNS CROGVITC Nh svt cadtatgein- ss ere ae sito restates eet nugsurey esa eager cease rpesh anther anet dato eebe asset 18 VET TOP SIS raarcpeacncaieds camaues totserssrberntanrtnsaxetareanonres costes ased oe Geshe se E Pep SOCEROTELUNEI Ec CPR 19 Dennettia, Monocyclanthus and flower variations in UvariopSis................. 19 The: “large leavesoroupesry 8 5b we et eet ee 20 New and under collected SpeCieS ..............ecsscccesseceesssseecsssseecseeesessnseeesenees 21 WV QTIOOET COM os.um wontes Siececercere fsbo trancunn 0A Ris oanaantd te debate teenie 23 East African Uvariodendron’s: an endless source of botanical discoveries....24 The morphological continuum of Uvariodendron fUSCUM..............c0ccccccee 26 The complexity of Uvariodendron MOIUNCENSE.............cccccccccceesseceeessseeeessees 28 Taxonomic revision of Dennettia, Uvariodendron and UvariopSis ..............006 29 TaxXKOMOMNCADISTORY. 088 cau terre pecectec spectros U8 anaoettavnaaec Matas os ae tees 29 UV ETI OD EIGN OR scar cx vx cesses smashes asa Pedeernuaeches wap tadses matua stents des decusuten erased taerigeeee 29 Pennetiatand IVanOpSiGn wae SA ie cally A eon leaded 30 Morphology and informative Characters ............ccccccsccssscccssceesseecssseeeeseeeeseeeeees 82 VEGETATIVE CIELACTONS) sorbet fone A Sader eae a Bee Re hata acaeh men votes Reonsne Mee 32 InfloreSCeNnces ANC FlOWETS...........cccceeccceesecsesseceesecesssecesseceeseceesseeesseeeeseeeesaes 33 Pollination anGrseed GiSDersal ...c::. 2d ccguuh Sesciet ct de Ueyeces teehee endear 35 EUDMOD OLE Yo iro. rene Mtr reteSleea ike ters erates eRe een cub lan tron abuse Ma MltaMns tle 36 MAXOMOMIUC WeAUM SNE cere. spsrsmcanrodecta2.coma rene ratpiacnnts traces Pelet nasi dies megmmnteretubisfossnces 36 (STi 16'/ O12) Ce | | ov = beaMesmamnent | Aaa eis OPE NTR ROMP Rt Sr ae Red ORME ol fons SNe Cake 36 Ophrypetaleae Dagallier & Couvreur, triD. NOV.............cccccccceesecceesesteeeeeeeens 36 Key to the genera of Monodoreae as recognized in this study .................... 36 PO CTAIG EELS a EMAC slice ons Ses cocstel eet ast, Betas na PAL sere caus er teaser cut eee bi bee tamer 37 Uvariodendron {Engli"&. Diels) R-EiEh eect dings cele esse needs 41 Key lO Van OCGERCFOM SPECIES i.) veasecl ta toed die saesecdhclendel seemed eicaeensewvess 41 SPECIES CESCIDUOMS Res upernsscenedn Madness vecas derek gteiewede deem ede ce onereeMavs 43 Uvariodendron angustifolium (Engl. & DielS) R.E.FT. .......ccccceeeeeseeeeeees 43 Uvanlodendronr-anisatum NeldG. 3.2050 & cctv vues ace decane eeeeeeaeees 46 UVaRIOGENGrON-GalO PAVE REE WE, cic s-eeccesevenezcgse er cetcsneametengaseevectoensaicen 50 Uvariodendron citriodorum (Le Thomas) Dagallier & Couvreur, COMPS Chota to NOV... AoA hecths..s ated mal ere Mien adele ndeer ent ees ea Mecnans 54 Uvariodendron connivens (Benth.) R.E.FT. ......cccccccceesecseeseeseeseeseeeeseeseesees 57 Uvariodendron dzomboense Dagallier, Q.Luke & Couvreur .................0008 62 Uvariodendron fuscum (Benth.) R.E.F ir. .......ccccccccscesecseeseeseeseeseeseeseeseesees 65 Uvariodendron fUSCUM Val. FUSCUM .........ccccccccccesseccececessceesseecesesessseeesaeens 66
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 3
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Uvariodendron fuscum var. giganteum (R.E.Fr.) Dagallier & Couvreur .....69 Uvariodendron fuscum var. magnificum (Verdc.) Dagallier & Couvreur, COND GE SEADM OWE Fes 98, tate a2 chon he eR sy ts cc nasa a aed raha esas ae pe UVAHODENGLOA-GOLIOOIS VLU Ce 8 occ ced seen caa dns seated Po cet bine vane encore 74 Uvariodendron kimbozaense Dagallier & Couvreur, Sp. NOV. ..........:::eee 79 UVATOGENGKOMATIN AI ONGC. = Sratecb rote canon brdea Muczes dies Aas h ack ante, Man bee Bon 82 Uvariodendron mbagoi Dagallier & COUVIEUF .............ceccceeeseecessseeeesseeeeeees 86 Uvariodendron molundense (Diels) R.E.FF. .........ccccccccccseceseescssesseseesseseeeees 89 Uvariodendron mossambicense Robson ex Dagallier & Couvreur, SPD INOWE 9 Fe sexaleasdciow ev egenemaseiaarh Mectacdvexeteas nomeyedeceseeteuiey anmee eet usaauneses an guenco crane 96 Uvariodendron occidentale Le Thoma................c:cccsssscecessecesessseeeesnseeeeenes 98 Uvariodendron pilosicarpum Dagallier & Couvreur, Sp. NOV. ...............008 101 Uvariodendron pycnophyllum (Diels) R.E.Fr. .......ccccccccccessesecsseeseeeesseseens 104 Uvariodendron schmidtii Q.Luke, Dagallier & COUVreUr .............: cece 107 Uvariodendron usambarense R.E.FT. .........cccsccccsssssccessseecesesesesseeeeessnseeees 109 UV AHO SIS. EMG): crcecccmmmeudmancantedeot rnc, seasben tesapleeauecrebaent,maihica se Secs Oeste aas Tetaces sf 12 Keyto Varo pSiS-SDCCIOS: sire easi/ ce lhesmeaenk eaniutnatabhcshs coe ussccentbonid eoutieakees 113 SPECIES CES CMOLIOMSs 5 he te alia oa aalus salons ate nn beg iad can dae nsdea gaa bbeaades tenes edgathere 115 Uvariopsis bakeriana (Hutch. & Daltz.) Robyns & Ghesq. ............ccc 115 WVAMOD SIS: DISEXHOU Se VENC ft. b.05, sent Mtie tescarncted tisiehectreums eat te cares 119 Uvarniopsis.citratast ouvreur&- NiagnG:=.). 74 achenk incertae 122 UVvanlopsis. CONGeNSIS-RODYNS & GMOS Ge or. cswcseesetecede.~taseereeles tein a eteraens 125 Uvariopsis congensis var. angustifolia Dagallier & Couvreur, var. nov. ....... 127 UVanOpsiS CONGENSIS-VARAGCONGENSIS.. 2se.tescrasezies cceaaseSedesttnnestidea tas flatten. 128 Uvariopsis congolana(De Wild.) FilGS 208.4 8.28 Aine. eects e Merce 130 Uvariopsis dicaprio Cheek & GOSIIN@ ......... ccc ccccccccsescceceesseeeeeeesssseeeeeneaas 133 Uvariopsis dioica (Diels) Robyns & Gh@SQ. ........cccecccceseescesecsseeeesseaees 135 Uvariopsis etugeana Dagallier & COUVICUF ..............cccccccccccesececeeesssseeeeeees 140 UVANMOD SISO HIM CENSISIKCAY: 3 585: secer eeenirshs -caesdenRasedantusconn Rwenkat aa ateeccsay eens 142 Uvariopsis guineensis var. globiflora (Keay) Dagallier & Couvreur, COMMBZ CL Stale MOM intake ins hs dena sttenseaheih tesckente cehuerssceel es achat ees sauee 146 Uvari0PSIS QUINEENSIS VAM. GUINGENSIS .............ccsesssccecececesesessnncceeceeeeeseseees 146 Uvariopsis korupensis Gereau & Kentack............cc:ccccsscceecssceeeesseeeeeseeeees 148 Uvariopsis lovettiana Couvreur & Q.LUKG .......c ccc cccccsssececeeeessseeeeeseaas 153 Uvariopsis noldeae Exell & MENdOnGa...............ccescesessteceesrsecesenseeeseeeeees Acy: Uvariopsis oligocarpa Dagallier & Couvreur, SP. NOV. ...........:ccccceeseeeeeees 159 Uvariopsis pedunculosa (Diels) Robyns & Ghe@SQ. .........cccccesecseesseeseeteees 163 Uvariopsis solheidii (De Wild.) Robyns & Gh@SQ. ..........cccccesceceseerseeeees 167 Uvariopsis solheidii var. letestui (Pellegr.) Dagallier & Couvreur, COMIN CE StA Ts MOMs 2 where ecerdts neers Peacoat keen where unente tenn orem nace sal east wes 170 Uvanopsis.SOlneiiiwar.S OLMCHOI xcs <2. e282. nanebesp it eSoe web dh ee besees eerste 12 Uvariopsis submontana Kenfack, Gosline & Gereau.............ccccceceeeeeeees 174 UVaTIOP SISAZ CHET MOM oe cccok a caedereesnceres meee arccnsu cote, en odode cumpedeeaiap erecstensii 178 UVAFODSIS-SD NOV IS WE ANC AN Scnsce Sees coae nheeace hatter Resarok wants cecanser Be 181 LIVAHODSIS-SD.NOV. 2 TANZAM as 201 5 ea OA eewt yeast rede arnypeaedaercan 182 UVAODSIS-SPANOV: B> CONGO 1 coc. citee cc sdutuensc auto Haase etoscacd az gigunbvessnenae 183 RETEREIC ES, coho ee sicenvries sashestt heaves eivanenigity ecssloanish enaactat ay nous eo leg duuty bestuvaniensaditusseecta'ses 186 SUPDISIIS MLA TALS DAUM ss scscdiode stn atets haneetdd et saleienssuecsints ae sanaatdiabelukecariedtuawens 198
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 4
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
SUDDIGINE NLA (MATS Mal Zier. seat eAN hno BEnd ABS th ica allel fat tion MP Ea eat remegeestrueteaas 199 SUPPIEIMEN LARVAE AS Fee corset ac teteatece ces Aaa ceaiet cen asedeapmesghdennssaeotaaden ei: 200 SUPPIEMENtaryaimate nla Ay). 0h nadeahnm bbeinschhnoesqlea ecerusbopacdaepianbelaaticeabenceshiee 200 Introduction
Annonaceae is a diverse pantropical family of trees, shrubs and lianas mostly restricted to tropical rain forests. Recent work based on molecular phylogenet- ics has classified Annonaceae into four subfamilies and several tribes (Chatrou et al. 2012; Guo et al. 2017a; Couvreur et al. 2019). Within the Annonoideae sub- family, tribe Monodoreae — previously referred to as the “African long-branch clade” (Couvreur et al. 2008a) — is composed of species distributed exclusively in tropical Africa and Madagascar. Before this study, the tribe was composed of 11 genera and ca. 90 species.
Monodoreae is a diverse clade of trees and small shrubs with one species (Monodora crispata) reported to be a lianescent (Couvreur 2009). Some gen- era, such as Uvariodendron, conform to the typical Annonaceae floral model of three sepals with alternating two whorls of three free petals, numerous free carpels (apocarpy) and bisexual flowers (van Heusden 1992; Couvreur et al. 2008b). In contrast, several genera within the tribe deviate from this pattern. For example, the genus Uvariopsis has dimerous flowers (two sepals and four petals) and individuals are unisexual, while the genera Asteranthe, Hexalobus, Isolona, Monodora, Sanrafaelia, and some species of Uvariopsis have fused inner and outer petals forming a single whorl. The genera /solona and Mono- dora have prezygotically fused carpels, i.e. syncarpous gynoecia, which is unique in Annonaceae (Deroin 1985; Couvreur et al. 2008b; Couvreur 2009). This important diversity renders a clear morphological circumscription of the Monodoreae tribe complicated. To date it has however been recognized by the combination of the mainly tree or shrub habit, indumentum of simple hairs, and especially sessile or shortly stipitate monocarps (Couvreur et al. 2008b; Chatrou et al. 2012). Most of the genera have been taxonomically revised (Couvreur 2009, 2014; Botermans et al. 2011; Gosline et al. 2019) except for the monotypic genera Monocyclanthus, Ophrypetalum and Sanrafaelia, and the genus Asteranthe with two species (Vollesen 1980). Recently, a new genus including two species, Lukea, was described from East Africa (Cheek et al. 2022). Morphologically, Lukea was suggested to be close to the Monodoreae genera Mischogyne and Monocyclanthus and thus potentially belongs to this tribe (Cheek et al. 2022).
In contrast to the recent taxonomic revisions cited above, recent revision- ary work for the two most diverse genera of the tribe, Uvariodendron and Uvariopsis, are more than 80 years old (Fries 1930; Robyns and Ghesquiére 1933a). Several new species were described since then (Verdcourt 1971a; Gereau and Kenfack 2000; Kenfack et al. 2003; Couvreur and Luke 2010; Da- gallier et al. 2021; Couvreur et al. 2022; Gosline et al. 2022) warranting a new taxonomic revision of both genera. The taxonomic history of Uvariopsis is complex with several expansions of the concept of the genus. For exam- ple, Kenfack et al. (2003) combined the monotypic genus Dennettia Baker f.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 5
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
into Uvariopsis, expanding the concept of this genus to having trimerous and dimerous flowers. This was supported by a molecular phylogeny based on few plastid markers (Couvreur et al. 2008a; but only included three species of Uvariopsis), and was recently contested based on morphological grounds (Cheek et al. 2022).
Reconstruction of phylogenetic relationships in species-rich clades such as Annonaceae is challenging. Several phylogenetic analyses have focused on the whole family (Doyle et al. 2004; Richardson et al. 2004; Guo et al. 2017a; Xue et al. 2020) or on particular tribes or genera (Couvreur et al. 2008a, b; Cou- vreur 2009; Thomas et al. 2012; Chaowasku et al. 2014; Tang et al. 2015; Guo et al. 2017b; Ortiz-Rodriguez et al. 2018). These phylogenies were reconstructed using few molecular markers (generally less than 10 chloroplast markers), al- though more recent studies included more and more markers (Guo et al. 2018; Lopes et al. 2018). In the Monodoreae tribe, phylogenetic relationships be- tween the genera have been inferred with relatively strong statistical support in several molecular phylogenetic studies based on a few chloroplast markers (Couvreur et al. 2008a; Guo et al. 2017a; Xue et al. 2020). These studies in- ferred three main clades, referred to here as: the “/solona clade”, (containing the genera Asteranthe, Hexalobus, Uvariastrum, Isolona, and Monodora), the “Uvariopsis clade” (containing the genera Uvariopsis, Monocyclanthus, Uvari- odendron, and Mischogyne), and the Ophrypetalum — Sanrafaelia clade (with just two species). This later clade was recovered as sister to the rest of the Monodoraeae tribe with moderate to strong support based on phylogenetic analyses of plastid markers. The development of phylogenomics in Annona- ceae (Couvreur et al. 2019) not only brought new insights to the understand- ing of the evolution of the family and of the tropical rain forests (Brée et al. 2020; Helmstetter et al. 2020a, b), but also clarified the systematics of the family. For example, the African genus Annickia was inferred to be excluded from Piptostigmateae, and erected as a new monogeneric tribe Annickieae (Couvreur et al. 2019). Some Monodoreae genera were also included in this study and in contrast to previous analyses (Couvreur et al. 2008a, b; Guo et al. 2017a), they found a strong phylogenetic affinity of Sanrafaelia to another tribe of Annonaceae, namely Uvarieae (Couvreur et al. 2019). This suggested that, based on a poor taxon sampling, the Ophrypetalum-—Sanrafaelia clade might not be part of Monodoreae.
Species level relationships within Monodoreae have only been inferred, based on few chloroplast markers, in /solona, Monodora and more recent- ly in Mischogyne (Couvreur 2009; Gosline et al. 2019) providing support to species and generic delimitation within the tribe. Moreover, the placement of Lukea within Monodoreae and the relationships in the species-rich Uvari- odendron and Uvariopsis genera have never been assessed with a near-com- plete taxon sampling.
The aim of the present study is to generate a robust species-level phylogenom- ic tree of the Monodoreae and test the limits between the genera and species. Given that the species rich genera Uvariodendron and Uvariopsis have never been fully assessed phylogenetically and taxonomically, we give a particular focus to these two genera and present a taxonomic revision of these two genera. We dis- cuss species delimitation based on both molecular and morphological evidence.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 6
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Materials and methods Taxonomic revision
We examined the morphological characters of the Monodoreae species based on the protologues of the species and on the taxonomic revisions of those genera that were available (Diels 1936; Keay 1953; Verdcourt 1960, 1996; Vollesen 1980; Couvreur 2009, 2014; Botermans et al. 2011; Gosline et al. 2019; Cheek et al. 2022). In addition, we examined numerous spec- imens of Uvariodendron and Uvariopsis, as well as several specimens of Monocyclanthus. The specimens came from B, BM, DSM, EA, G, K, M, MO, MPU, P, WAG and YA herbaria (herbaria acronyms follow Thiers 2016). The high quality scans of some additional specimens or sheets from A, BR, BRLU, COI, E, FHO, GOET, HBG, L, LE, MA, MHU, S, US, WU and Z were also examined, as well as pictures taken in the field or personal fieldwork ob- servations. For the type specimens, an exclamation mark (!) is appended stating either the specimen itself or a high quality scan was seen. Additional duplicates from herbaria not listed above might appear in the lists of speci- mens, but these were not seen and are cited for information. The format for the list of specimens follow recommendations from Bénichou et al. (2018) and includes a bullet point (*) at the beginning of each specimen to visually ease the reading.
When a holotype was composed of several sheets from a same gathering within a herbarium, we designated a single sheet as holotype (identified by its barcode) with the mention ‘sheet here designated’. The other sheets were listed as isotypes. This was done for all names except when the protologue explic- itely specified that the holotype is composed of several sheets from a same gathering within a herbarium (e.g. Uvariodendron fuscum var. magnificum),
Measurements, colors and other details given in the descriptions are based on living material, spirit and herbarium specimens, and data derived from field notes. Morphological descriptions followed terminologies from Hickey et al. (1999) and the Systematics Association Committee for Descriptive Biologi- cal Terminology (1962) for leaf and plane shapes, Payne (1978) for the indu- mentum, and Harris and Harris (2001) for the other terms. To characterise the seeds, we used the term ‘semicircular’ to describe the three dimensional shape of a semicircle, like a D-shaped ellipsoid (see e.g. Fig. 29H). We used custom scripts inspired by the exsic (Simon and Spooner 2013) and monographR (Regi- nato 2016) packages in R 4.1.3 (R Core Team 2022) to automatically generate initial species descriptions and specimens’ citations.
For this work, we applied a combination of the phylogenetic and morpho- logical species concept. Thus, a species is recognized if it has support for monophyly and if it exhibits morphological characters that can differentiate it from the others. We also recognized varieties (or sunk previously described species into varieties) when a difference of morphology could be identified, but no monophyly was recovered by the phylogenetic analyses. In some cases, we recognized varieties even if they present an overlap in some of the morpholog- ical characters used to differentiate them. This is to recognize the existence of different morphological groups (or “archetypes”) in the morphological varia- tion of the species. This reflects the uncertainty around the species, given the
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
material available. The collection of additional material will certainly provide a better understanding of these morphologically complex groups.
To avoid ambiguities, when necessary, the names Uvariodendron and Uvariopsis were abbreviated to Ud. and Up., respectively.
IUCN assessments were retrieved from https://www.iucnredlist.org/ (ac- cessed 21 September 2022). For species not present in the Red List, we made a preliminary conservation status assessment. We calculated the extent of occurrence (EOO) and the area of occupancy (AOO) using the ConR package (Dauby et al. 2017) and followed IUCN Red List Categories and Criteria Version 3.1 (IUCN 2012) to assign a preliminary conservation status. For the distribu- tion of the species, we specify the country(ies) in which they are distributed, as well as their chorological classification. The chorological part follows White (1979, 1983, 1993) but simplifies the chorological categories (“regional (sub) centre of endemism” and other) into Region and Domain.
Phylogenomics Taxon sampling
We sampled at least one specimen for every species of the Monodoreae tribe, several specimens from the Uvarieae tribe representing different gen- era, as well as several other Annonaceae outgroups (Chatrou et al. 2012; Suppl. material 3). Within Monodoreae, we sampled, when possible, more than one specimen per species following these cases: one specimen per subspecies or variety; one specimen per major geographic region for wide- spread species (between East Africa, West Africa, Central Africa); several specimens for morphologically variable species representing that variability (Suppl. material 3).
For all specimens, DNA was extracted from either silicagel dried leaf sam- ples or leaf material taken from herbarium specimens. Details about speci- mens and vouchers are available in Suppl. material 3.
For the downstream analyses, every sample was assigned a unique identifier as follow: RUN_##_l##_T##_Genus_species-COL_NUM. “RUN_##_l##_T##’ is the identifier used for the sequencing process and bioinformatics analyses. “Genus_species” is the most up to date taxonomic identification of the speci- men (i.e. after applying the taxonomic changes treated in this paper). To ease the reading of updated names, some of the specimens have their old identifi- cation in parentheses like “Genus_species_(ex_old name)”. “COL_NUM’” is the three first letters of the name of the collector and the number of collection of the specimen (e.g. “VAL_2540” stands for the specimen n°2540 collected by J.L.C.H van Valkenburg). The details about every sample can be found in the Suppl. material 3.
DNA extraction, library preparation and sequencing
DNA extraction and NGS library preparations for nuclear exon capture followed Couvreur et al. (2019). Libraries were sequenced using an Illumina HiSeq 2000 plateform using paired-end sequencing of length 150 bp by Novogene Co. Ltd.
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Raw sequence bioinformatics
Raw read sequences were demultiplexed using the demultadapt script (https:// github.com/Maillol/demultadapt). Adapters were removed from the reads using cutadapt 1.18 (Martin 2011) with the “-b” option and the “-O 7 -m 35 -q 20 -e 0.1” parameters. Low quality reads were then excluded (mean quality phred score below 30 and read less than 35 bp long) using a script modified from https:// github.com/SouthGreenPlatform/arcad-hts/blob/master/scripts/arcad_hts_2_ Filter_Fastq_On_Mean_Quality.pl. Reverse and forward reads were paired ac- cording to their names in the fastq files using a custom script (https://github. com/SouthGreenPlatform/arcad-hts/blob/master/scripts/arcad_hts_3_syn- chronized_paired_fastq.pl). A final step of 6 bp trimming was performed on the reverse reads using FASTX-Toolkit (https://github.com/agordon/fastx_toolkit).
Contig assembly and alignment
To process the clean reads, we used the HybPiper v1.3.1 pipeline (Johnson et al. 2016) following Couvreur et al. (2019). This pipeline mapped the reads on to the targeted nuclear exons using BWA v0.7.12 (Li and Durbin 2009). The mapped reads were assembled into contigs using SPAdes v3.11.1 (Bankevich et al. 2012). Overlapping contigs were then assembled into ‘supercontigs’ containing both targeted sequence (i.e. exon) and off-target sequence data (i.e. partial in- tron). The pipeline ends up with one file per gene (supercontig) containing the sequence for every individual. The sequences were then aligned for each gene using MAFFT v7.305 (Katoh and Standley 2013) using the automatic selection of the alignment algorithm (--auto). Alignments were trimmed with Gblocks 0.91b (Talavera and Castresana 2007), to remove poorly aligned regions.
Phylogenetic reconstruction
We used two different approaches for the phylogenetic reconstruction: the con- catenation approach and the gene tree approach. For each approach, we first re- moved the supercontigs that were putatively identified as paralogs within the Hyb- Piper pipeline, and then filtered our dataset to select only the supercontigs that are present in 75% of the individuals and for which the sequence contains at least 75% of the length of the target sequence (75/75 filter, following Couvreur et al. 2019).
Concatenation approach
For each supercontig, the alignments were filled with gaps and missing indi- viduals so that every sequence in the alignment has the same length and every alignment contains all the individuals. The alignments were then concatenat- ed into a single “supermatrix” using the pxcat function in the phyx program (Brown et al. 2017). A phylogenetic tree was inferred from the supermatrix us- ing an optimized maximum likelihood (ML) tree search implemented in RAXML 8.2.9 with the GTRGAMMA model after a rapid bootstrap analysis (Stamatakis 2014). We specified Anaxagorea crassipetala as an outgroup (“-o” option) and constrained the ML search on a backbone topology (“-g” option), in order to
a n”
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 9
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe — Revision of Uvariodendron and Uvariopsis
avoid long-branch attraction due to the scarce sampling of the outgroups. The backbone topology only includes the outgroup species and follows the results of Couvreur et al. (2019): (Anaxagorea_crassipetala-MAA_9408, (((((Uvarioden- dron_kirkii-DAG_09, Uvaria_grandiflora-COU_838), Annona_glabra-CHA_467), Duguetia_staudtii-COU_1014), Guatteria_jefensis-MAA_9553), Greenwayoden- dron_suaveolens-COU_746)).
Gene trees approach
We inferred a phylogenetic tree for every supercontig using RAXML 8.2.9 (Sta- matakis 2014) under the GTRGAMMA model and 100 bootstrap replicates. For every tree obtained, we removed the branches with a bootstrap support less than 10% using the Newick Utilities program (https://github.com/tjunier/ne- wick_utils), in order to improve the accuracy of the inferred species tree (Zhang et al. 2018). We then inferred the summary species tree from all the (unrooted) genes trees using ASTRAL-III 5.7.5 under the multi-species coalescent model (Zhang et al. 2018, 2018). The support at the branches was estimated both with the quartet support (QS) values (“-t 1” option) and with the local posterior probabilities (LPP) (default parameters). The species tree was then rooted on Anaxagorea crassipetala (Anaxagorea_crassipetala-MAA_9408). The phyloge- netic trees obtained were then plotted and annotated using the ggtree, ggplot and treeio packages (Wickham 2016; Yu et al. 2017; Wang et al. 2020).
Results Specimens examined
In total, we examined ca. 1,500 herbarium sheets, representing 928 herbari- um specimens, including 486 of Uvariodendron, 405 of Uvariopsis, 35 of Den- nettia, seven of Monocyclanthus and two of Lukea (Suppl. material 4, https:// doi.org/10.15468/zdvvkh). We compiled the morphological characters of the Monodoreae genera in the Table 1.
Phylogenomics
A total of 464 exon regions were recovered out of the 469 contained by the Annonaceae baiting kit (Couvreur et al. 2019). Of these, 39 exon regions were identified as potential paralogs using HybPiper. After discarding the potential paralogs and applying the 75/75 filter (see Methods), the dataset comprised 334 supercontigs. This subset was used for the downstream phylogenetic analyses with both the concatenation (after concatenation to a supermatrix) and gene trees approaches. After alignment, the supercontigs ranged in length between 131 and 9422 distinct sites (mean: 1,234; median: 844). After concat- enation of the 334 supercontigs, the supermatrix totaled 449,445 distinct sites.
Phylogenetic relationships
At the genus level and above, we recovered the same topology with both the gene tree (ASTRAL) and the concatenation (RAxML) approaches (Fig. 1, Sup-
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 10
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
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PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
pl. materials 1, 2) with high levels of statistical support. The local posterior probabilities (LPP) were all above 0.9, the quartet supports (QS) were gen- erally high, and the bootstrap (BS) values were all 100%. The Ophrypetalum - Sanrafaelia clade is retrieved as sister to the Uvarieae with maximum BS and LPP support but with relatively low QS (44%) (Fig. 1, Suppl. materials 1, 2). All the genera were retrieved as monophyletic, except Uvariopsis for which the species Uvariopsis tripetala clustered as sister to Monocyclanthus (Fig. 1, Suppl. materials 1, 2). The two species of the newly described genus Lukea clustered together, as sister to Mischogyne with strong support. The branch leading to the crown node of Mischogyne was relatively long (Fig. 1, Suppl. materials 1, 2).
Species monophyly within the genera Asteranthe, Hexalobus, Lukea, Mischo- gyne, and Monocyclanthus received strong support, and the relationships be- tween species were generally strong (BS > 90%, LPP > 0.9) and similar between both phylogenetic approaches (Fig. 1, Suppl. materials 1, 2). In Hexalobus, the three specimens of Hexalobus monopetalus sampled from different countries (from Senegal, Mozambique and Angola) clustered together (Fig. 1, Suppl. ma- terials 1-3) despite the species being widespread.
In Isolona, Monodora, Uvariastrum, Uvariodendron and Uvariopsis, there are incongruences in topologies between the RAXML and the ASTRAL trees, and the node support is generally strong (BS > 90%, LPP > 0.9), but some nodes are weakly (BS < 70%, LPP < 0.7) to moderately supported (70% < BS < 90%, 0.7 < LPP < 0.9) (Fig. 1, Suppl. materials 1, 2).
In Uvariastrum, U. pierreanum and U. insculptum are strongly supported as monophyletic, but U. zenkeri is recovered as paraphyletic. The species U. ger- mainii is retrieved as sister to U. pierreanum with moderate to strong support in both approaches. U. insculptum is retrieved as sister to all the other species in the genus (Fig. 1, Suppl. materials 1, 2).
In Uvariodendron and Uvariopsis, most species were recovered as mono- phyletic (Fig. 1, Suppl. materials 1, 2), but in some cases we appear to have a species complex, that is either a cluster of closely related individuals from more than one species, or separate clusters of individuals from a single spe- cies (Sigovini et al. 2016). In Uvariodendron, the specimens identified as Ud. gi- ganteum (Couvreur 1057 and Couvreur 1206) and Ud. magnificum (Hamilton 676) are nested in a clade with the specimens identified as Ud. fuscum, and the branches subtending Ud. fuscum specimens are generally weakly supported in both RAxML and ASTRAL trees (Fig. 1, Suppl. materials 1, 2). The specimens previously identified as Ud. molundense clustered together, but formed three genetically distinct and strongly supported groups: one including the single specimen Sosef 2219, previously identified as Ud. molundense var. citrata, sis- ter to the other two groups, another one composed of specimens Sosef 2261 and Valkenburg 2540, and a final group composed of the remaining sampled specimens. The three groups are separated by relatively long branches, espe- cially the group formed by the specimens Sosef 2261 and Valkenburg 2540 (Fig. 1, Suppl. materials 1, 2).
In Uvariopsis, the crown node of the clade formed by Up. bakeriana, Up. citra- ta, Up. korupensis, Up. submontana (« large leaves » group on Fig. 1) is strongly supported, but forms a species complex: while Up. bakeriana is retrieved as monophyletic with strong support (Fig. 1, Suppl. materials 1, 2), Up. korupen-
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
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Monodoreae
Figure 1. Phylogenetic trees of the Monodoreae inferred with ASTRAL, based on 334 nuclear genes trees. The branch support is given as local posterior probability (LPP) in three shades of greys. For the details on the specimens see Suppl. material 3. Insets: flowers of A Ophrypetalum odoratum (Couvreur 82) B Sanrafaelia ruffonammari (Dagallier 31) C Aster- anthe asterias (Dagallier 10) D Hexalobus crispiflorus (no specimen associated) E Uvariastrum zenkeri (no specimen as- sociated) F Isolona hexaloba (no specimen associated) G /. cauliflora (Dagallier 44) H Monodora grandidieri (Dagallier 26) I M. myristica (living specimen at NY conservatory) J M. tenuifolia (Couvreur 1019) K Mischogyne elliotana (no specimen associated) L Uvariodendron gorgonis (Dagallier 38) M Ud. molundense (Bidault 2222) N Ud. connivens (Couvreur 1016) O Ud. var. fuscum (Couvreur 990) P Uvariopsis congensis (Lachenaud 1384) Q Up. lovettiana (Couvreur 97b) R Up. baker- iana (Couvreur 1000) S Up. submontana (Couvreur 627) T Up. pedunculosa (Couvreur 878). Photos CC BY-NC 4.0 A, D-F, J, N, 0, Q-T Thomas Couvreur B, C, G-I, L Léo-Paul Dagallier K Carel Jongkind M Ehoarn Bidault P Olivier Lachenaud.
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sis is retrieved as paraphyletic in both phylogenetic approaches (Fig. 1, Suppl. materials 1, 2), while Up. citrata is retrieved as monophyletic with moderate support in the gene tree approach only (QS < 50%, LPP < 0.7).
Discussion
Phylogenomics of the Monodoreae tribe
We provide here (Fig. 1, Suppl. materials 1, 2) the first complete species level phylogenomic reconstruction of the Monodoreae tribe based on 334 nuclear loci using a targeted sequencing approach (Couvreur et al. 2019). Indeed, we sequenced all of the 90 currently accepted species, and included the speci- mens of three potentially new species. Such a level of species sampling with hundreds of nuclear markers has never being achieved for a diverse tribe of Annonaceae to date. Couvreur et al. (2019) published a species level phy- logenomic study using the Annonaceae baiting kit of tribe Piptostigmateae, but this study included 74% of know species in the tribe (Brée et al. 2020). In addition, we were also able to sample several specimens within species to test species limits and concepts. Our high level of inter- and intra-specific sampling for Monodoreae was possible thanks to the successful sequenc- ing of DNA extracted from herbarium specimens. Indeed, 49% (101/207) of specimens sequenced in this study were sampled from herbarium specimens, versus 51% (106/207) available from different silicagel DNA banks. Four spec- imens included here were more than 110 years old dating back to 1898, 1900, 1910 and 1911. Our results underline once again the central importance of herbarium specimens for phylogenetic inference (Bebber et al. 2010; Bakker 2019; Brewer et al. 2019) of tropical plants, in particular to achieve high levels of taxon sampling needed to test species limits but also infer more accurate macroevolutionary patterns.
Generic level relationships within Monodoreae generally agree with molecu- lar phylogenies based on few plastid markers (Couvreur et al. 2008a; Chatrou et al. 2012; Guo et al. 2017a). There are however, two major differences when compared to plastid data: the position of the two east African genera Ophry- petalum and Sanrafaelia not being sister to the rest of Monodoreae, and the position of the species Uvariopsis tripetala. These differences and taxonomic implications are discussed in detail below.
Even though sequencing of hundreds of markers combined with a dense tax- on sampling appear as a silver bullet to understand species limits, it doesn’t al- ways provide clear cut answers. Indeed, phylogenetic conflicts are common in plant systematics: incongruences can occur between concatenation and gene tree approaches (Shen et al. 2021), or reconstructions based on nuclear loci versus chloroplast loci (Morales-Briones et al. 2018). Such incongruences are often attributed to reticulate processes of evolution occurring at the population level, like horizontal gene transfer, hybridizations or incomplete lineage sort- ing (ILS) (Maddison 1997; Naciri and Linder 2015; Morales-Briones et al. 2018; Schrempf and Szdllési 2020). Phylogenetic conflict, associated with little di- vergence between species, is also known to coincide with rapidly evolving taxa in case of adaptive radiations (Meyer et al. 2017) and morphological innova- tions (Parins-Fukuchi et al. 2021). Widespread species can also be retrieved
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
as non-monophyletic, with diverging range-restricted species embedded within them. This is due to the retention of ancestral polymorphisms in widespread species where both the population size and the generation time are too high to achieve complete lineage sorting from the divergence time until the present day (Pennington and Lavin 2016). This has been documented in Amazonia where tree species restricted to seasonally drought-affected forests are retrieved em- bedded in rain forests tree species (Pennington and Lavin 2016). These pro- cesses at the population level might be the cause of the observed phylogenetic conflicts in /solona, Monodora, Uvariastrum, Uvariodendron, and Uvariopsis, and likely explain the species complex in the later two genera. Nevertheless, our study provides a solid phylogenetic framework to test different relationships within this tribe, confirming some and disagreeing with previous results. Below we discuss our results from a taxonomy point of view.
Re-circumscription of the tribe
The two monotypic sister genera from East Africa, Ophrypetalum Diels (Kenya and Tanzania) and Sanrafaelia Verdc. (Tanzania) (Diels 1936; Verdcourt 1960, 1996), called the Ophrypetalum-Sanrafaelia clade here, were informally linked to some genera (i.e. the Hexalobus group, Asteranthe, Hexalobus, Isolona, Monodora) now placed in Monodoreae based on floral morphology (van Heu- sden 1992). Phylogenetic studies at the genus level and based on few chloro- plast markers recovered these two genera as sister to all the other Monodoreae genera with moderate to strong support (Couvreur et al. 2008b; Chatrou et al. 2012; Guo et al. 2017a; Xue et al. 2020). Here, with more than 300 nuclear loci and a much denser species level sampling, we retrieved both genera as sister to the Uvarieae tribe, with strong support (Fig. 1, Suppl. materials 1, 2). Our analyses thus confirm the result of Couvreur et al. (2019) using the same bait- ing kit, but only sampling Sanrafaelia and fewer species within Monodoreae. The discrepancy between the relationships inferred in the previous studies and here can be attributed to the higher number of loci and species sequenced, but also to the use of nuclear vs. chloroplast loci.
The Ophrypetalum-—Sanrafaelia clade share several morphological charac- ters also found in other Monodoreae genera (Fig. 2), in addition to occurring in tropical Africa, such as being trees with simple indumentum, monocarps (in- dividual fruiting units) that are sessile or shortly stipitate (stipes shorter than 10 mm) or pollen units forming tetrads (except for /solona (monads)) (Couvreur et al. 2008b). The morphological link to tribe Uvarieae based on morphological grounds is harder to make. Uvarieae is mainly composed of genera having a lianescent habit, except for Cleistochlamys (East Africa) and Dasymaschalon (South East Asia) which are trees or shrubs (Verdcourt 1971a; Wang et al. 2009, 2012). In addition, most species have an indumentum of stellate hairs (more rarely simple in some Uvaria species) and fruits with generally stipitate monocarps and pollen in monads (Couvreur et al. 2008b; Chatrou et al. 2012; Doyle and Le Thomas 2012). Likely most of these characters are novelties for the Uvarieae, while both the Monodoreae and the Ophrypetalum-—Sanrafaelia clade show the plesiomorph condition. This precludes Ophrypetalum and San- rafaelia as being part of Uvarieae based on morphology alone. This distinction from the tribe Uvarieae is also supported genetically by the long branches sus-
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Figure 2. Ophrypetaleae tribe. Ophrypetalum odoratum Diels A trunk B young branch with leaves, upper side C flower and flower buds D flower, from below. Sanrafaelia ruffonammari Verdc E trunk F young branch with leaves and flower buds G flower buds H flower, top view I flower, side view J fruit. A, B Dagallier 54 C Couvreur 56 D Couvreur 82 E-J Dagallier 31. Photos A,B, E-J Léo-Paul Dagallier C, D Thomas Couvreur.
taining the Ophrypetalum-—Sanrafaelia clade from the crown node of Uvarieae (Fig. 1, Suppl. materials 1, 2). We thus propose the erection of the new tribe Ophrypetaleae to accommodate these two genera. The description of the new tribe is provided in the Taxonomic treatment section below. Interestingly, both genera are quite different in terms of flower morphology (Verdcourt 1971a, 1996). Ophrypetalum has two whorls of three free petals, with the inner ones clawed and presenting a small brush-like appendage on the inner side and has numerous carpels (10-15) (Fig. 2A-D). In contrast, Sanrafaelia has six petals united into a single whorl and has a single carpel (Fig. 2E-J). These differences
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between sister genera underline once again the great morphological diversity of African genera probably linked to differences in pollination vectors (Gotts- berger et al. 2011).
After our study presented here, the tribe Monodoreae is composed of 11 genera and 90 species, and the main morphological characters are provide in Table 1.
Asteranthe
Asteranthe is an East African genus characterised by large fleshy flowers with basally fused petals and numerous free carpels (Verdcourt 1971a). Asteran- the was strongly supported as monophyletic (Fig. 1, Suppl. materials 1, 2), and recovered as sister to the mainly central African genera Hexalobus and Uvari- astrum confirming previous analyses (Couvreur et al. 2008a). The name Aster- anthe trollii Diels (Diels 1936) was synonymized by Verdcourt with Asteranthe asterias (S. Moore) Engl. & Diels (Verdcourt 1971a). Verdcourt argued that the type species of A. trollii was very similar to A. asterias (Verdcourt 1971a, b). Here, we sequenced the specimen Luke 7641, originally identified as A. trollii, which clustered with the other sampled specimens of A. asterias (Fig. 1, Suppl. materials 1, 2). Thus, even though we did not sequence the type specimen, our results support the synonymy proposed by Verdcourt (1971a, b).
In addition, Verdcourt (1971a) described the subspecies Asteranthe asterias subsp. triangularis based on the petals being narrowly triangular (vs. linear-ob- long to linear in Asteranthe asterias subsp. asterias). In our analysis, both sub- species are genetically separated but sister groups (Fig. 1, Suppl. materials 1, 2), supporting Verdcourt's proposal. However, sampling more specimens of A. asterias subsp. triangularis would be necessary to decide whether the sub- species should be erected to the species level.
Hexalobus
The genus Hexalobus contains five accepted species (Botermans et al. 2011). This genus is characterized by basally fused petals which are longitudinally fold- ed (wrinkled) in bud, a character unique within the family (van Heusden 1992; Botermans et al. 2011). The species H. monopetalus has a very widespread “ring” type distribution, from Senegal to the north of South Africa (and parts of Angola). It occurs in drier woodland savannah or gallery forests (Botermans et al. 2011). This is unique among the Monodoreae species, which generally have ecological affinities with wetter areas and have a more restricted geograph- ical distribution. Our geographically widespread sampling of H. monopetalus (three specimens from Angola, Mozambique and Senegal) was recovered as monophyletic with strong support (Fig. 1, Suppl. materials 1, 2), confirming that despite its widespread distribution, it is a single species. In addition, H. monop- etalus is inferred as sister to the other dry adapted species of the genus H. mo- sambicensis (Botermans et al. 2011).
The widespread central African species H. crispiflorus is recovered as sis- ter to the more narrowly distributed H. salicifolius (Cameroon and Gabon) with maximum support in both analyses (Fig. 1, Suppl. materials 1, 2). This confirms they are closely related as suggested by Le Thomas (1969). They do however
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differ by several morphological characters such as smaller leaves and smooth- er monocarps in H. salicifolius. Monophyly, however, needs to be confirmed by a denser sampling within each species.
Uvariastrum
Uvariastrum is a genus containing five accepted species characterized by redu- plicate-valvate (i.e. curved outwards) sepals margins (Couvreur 2014). Morpho- logically, the five species are clearly differentiated based on several characters such as the indumentum and leaf morphology. Our results, however, underline some level of phylogenetic conflict (Fig. 1, Suppl. materials 1, 2). The geograph- ical distributions of all the species overlap, at least partially, in central Africa, except for U. hexaloboides that is distributed in Zambia and in Katanga region (south Democratic Republic of the Congo) (Couvreur 2014). The lack of sup- port for the nodes subtending U. zenkeri and U. germainii could be caused by old or occasional hybridization between the species but the inter-fertility has never been accounted for for any of the Uvariastrum species. Another expla- nation is that they diverged too recently to exhibit much differentiation at the molecular level (Erkens et al. 2012).
The case of the newly described genus Lukea
Recently, the genus Lukea Cheek & Gosline was described, endemic to East Africa with two species: Lukea quentinii Cheek & Gosline and Lukea trici- ae Cheek & Gosline (Cheek et al. 2022). Morphologically, Lukea resembles Mischogyne by the finely reticulate tertiary venation of the leaves and the absence of connective shield on the stamens (Gosline et al. 2019). Lukea presents a bowl-shape calyx persisting in fruit, a character unique within the Monodoreae tribe, although resembling the fused sepals found in Monocy- clanthus (Cheek et al. 2022) and in Uvariodendron schmidtii W.R.Q. Luke, Da- gallier & Couvreur (Dagallier et al. 2021). Our results recovered Lukea quentinii as sister to Lukea triciae, and the whole genus Lukea as sister to Mischogyne, with great genetic divergence (Fig. 1, Suppl. materials 1, 2). This supports the genus level status of Lukea, and its inclusion in Monodoreae as suggested previously (Cheek et al. 2022).
Mischogyne
Mischogyne is a genus of five accepted species characterized by the combina- tion of different morphological features such as prominent reticulate tertiary veins and carpels touching each other at their base but separated at their apex (Gosline et al. 2019). The clade formed by M. congensis and M. micheloides is consistent in both our analyses (Fig. 1, Suppl. materials 1, 2) and with pre- vious phylogenetic work on the genus based on a few plastid locus (Gosline et al. 2019). The position of the East African species M. idii remains however uncertain, either retrieved as sister to the clade M. congensis—M. micheloides (Gosline et al. 2019), sister to M. gabonensis (Fig. 1, Suppl. materials 1) or to M. elliotana (Suppl. materials 2).
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Uvariopsis
Uvariopsis Engl. is one of the most diverse genera of the Monodoreae tribe with 17 currently accepted species and until recently, several species were unknown to science (Couvreur and Luke 2010; Couvreur and Niangadouma 2016). Morphologically, Uvariopsis is characterised by monoecious individuals (separate male and female flowers on a single individual) and by exhibiting a type of flower uncommon in Annonaceae, composed of two sepals and four petals (Robyns and Ghesquiére 1933a). Uvariopsis congolana (De Wild.) Fries however has two sepals and three petals (De Wildeman 1909). Uvariopsis con- golana was previously described under a different genus name (Thonnera De Wild.), but was later combined into Uvariopsis (Fries 1953). Both our molecular phylogenetic analyses retrieved Up. congolana as sister species of Up. dioica with strong support (Fig. 1, Suppl. materials 1, 2), confirming its placement within Uvariopsis. In 1986, Verdcourt described the species Up. bisexualis from Tanzania, having the typical Uvariopsis flower with two sepals and four petals (and other typical pollen microscopic characters, see Verdcourt (1986)), but with bisexual flowers, thus extending the concept of the genus as also having bisexual flowers (Verdcourt 1986).
Dennettia, Monocyclanthus and flower variations in Uvariopsis
In 1913, Baker described the monotypic genus Dennettia Baker f., with a sin- gle species Dennettia tripetala Baker f. having bisexual flowers with “2 rarely 3 sepals” and three petals in a single whorl (Baker 1913). In 2003, Kenfack et al. combined the genus Dennettia into the genus Uvariopsis under the name Uvariopsis tripetala (Baker f.) G.E. Schatz, based on four main arguments (Ken- fack et al. 2003). First, the morphological circumscription of Uvariopsis had been extended to also include bisexual flowers by Verdcourt (1986, Up. bisexu- alis); second, Kenfack et al. (2003), observed specimens of D. tripetala exhibit- ing flowers with 2 sepals and 4 petals, thus reminding of the typical Uvariopsis flower; third, Kenfack et al. (2003) considered that because Up. congolana has 3 petals, the number of perianth segments is unreliable as a generic distinction for Uvariopsis; and fourth, the pollen microscopic features of D. tripetala are very close to those of Uvariopsis (Kenfack et al. 2003; Doyle et al. 2004). This was initially confirmed based on molecular phylogenetic analyses using few plastid regions, recovering Uvariopsis tripetala as nested within Uvariopsis but based on just three species sampled within Uvariopsis (Couvreur et al. 2008a; Chatrou et al. 2012).
After careful examination of 16 flowering specimens identified as Uvariopsis tripetala (including the type Dennett 44), we found that this species invariably exhibits 3 sepals and 3 petals. The sepals are fused at the base up to more than half of their length, forming a ring curved downward and persisting on the fruiting pedicel. In some rare cases we observed that the lobes of the calyx (i.e. the free parts at the apices of the basally fused sepals) are sometimes almost inconspicuous on the fruiting pedicel, allowing for the confusion with a two sepal-like calyx. To date, and based on the specimens we observed, we haven't seen any flowers of Up. tripeta/a with four petals, contrary to the affirmation of
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Kenfack et al. (2003). If such flower arrangements exist, they must be extreme- ly rare. It is also possible that the four petal flowers observed by Kenfack et al. (2003) were actually flower buds of the new species, Uvariopsis oligocarpa Da- gallier & Couvreur (see the Taxonomic Treatment section), as their geographic ranges overlap and leaves are quite similar (but Up. oligocarpa is unisexual). In contrast to the previous phylogenetic analyses, we did not recover Dennettia (Uvariopsis) tripetala as nested within Uvariopsis, but as sister to the monotypic West African genus Monocyclanthus vignei Keay, with strong support in both phylogenetic approaches (Fig. 1, Suppl. materials 1, 2). Dennettia (Uvariopsis) tripetala differs from Monocyclanthus vignei (Keay 1953) by having three petals in one whorl (vs. six petals in one whorl), the lobes of the fused sepals generally distinct (vs. generally inconspicuous), and a receptacle height:width ratio less than 1, i.e. wider than tall (vs. a receptacle height:width ratio greater than 1, i.e. taller than wide) (see Table 1). The single whorl of six petals of Monocyclanthus supposedly results from the compression of separate ancestral whorls (Saun- ders 2010). For Dennettia, the single whorl of three petals might result from a similar compression of separate ancestral whorls followed by a loss of petals, or from the loss of a whorl of petals.
All these morphological and phylogenetic elements suggest that Dennet- tia (Uvariopsis) tripetala is part of neither the genus Uvariopsis nor the genus Monocyclanthus. We thus reinstate the monotypic genus Dennettia, with its sin- gle species Dennettia tripetala Baker f. (see Taxonomic treatment). This was also suggested previously by Cheek et al. (2022) based on morphology.
Given the above, the morphological circumscription of Uvariopsis must be reevaluated. Uvariopsis was generally circumscribed as having 2 sepals and 4 petals (Kenfack et al. 2003). However, Uvariopsis congolana differs from all other Uvariopsis species by having flowers with 3 petals instead of 4. Uvariopsis congolana was successfully sequenced and nested within Uvariopsis with strong support (sister to Up. dioica, Fig. 1, Suppl. materials 1, 2). Thus, the number of petals (4 versus 3) is not a good diagnostic character for Uvariopsis. However, Up. congolana has 2 sepals, similarly to all the other Uvariopsis species, making this character a good synapomorphy for the genus. The synoptic characters of the genus Uvariopsis Engl. are given in the Taxonomic Treatment section below.
The “large leaves” group
Based on our dense taxon sampling, we identified a group of closely related species for which the phylogenetic limits remain uncertain. Indeed, the four species Up. bakeriana, Up. citrata, Up. korupensis and Up. submontana clus- tered as monophyletic with strong support (Fig. 1, Suppl. materials 1, 2), but support for the monophyly of each individual species and the relationships between them remains ambiguous (Fig. 1, Suppl. material 2) with some gene tree conflict (Suppl. material 1). They share some morphological characters in particular the large size and shape of their leaves, hence referred to as the “large leaves” group here. They are all trees with large obovate leaves (up to 30-60 cm long) having rounded to cordate bases, and display flowers borne along the trunk with varying degrees on density, from densely packed in Up. sub-
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montana to sparsely distributed in Up. citrata (Kenfack et al. 2003; Couvreur and Niangadouma 2016). In addition, flowering pedicels are shorter than 7 cm and petals generally 3 to 10 times longer than wide. Despite these similarities, they differ by several marked characters. Uvariopsis bakeriana is characterized by its unique petals that are narrowly ovate to linear and bright pinkish to deep red in color (Hutchinson and Dalziel 1927b). Uvariopsis citrata is characterized by its leaves emitting a strong lemon scent when crushed and sessile flowers (Cou- vreur and Niangadouma 2016). Uvariopsis korupensis and Up. submontana have similar flowers with pedicels generally 20-70 mm long, ovate to narrowly ovate shortly fused at base, but are differentiated by their ecology (Up. korupen- sis occurs below 200 m, Up. submontana above 900 m), the degree of flowers density on the trunk (less densely clustered in Up. korupensis) and the sepals being smaller in Up. korupensis (1-5(7.5) mm long) than in Up. submontana (5-11 mm long) (Gereau and Kenfack 2000; Kenfack et al. 2003).
Based solely on the phylogeny, this group could be considered as a single species. However, given the morphological differences of each species detailed above we choose to keep the taxonomy of this group as it is. Phylogenetic con- flict is known to be coincident with morphological innovations (Parins-Fuku- chi et al. 2021), as observed in recent and fast diverging groups (Meyer et al. 2017). Here we retrieve such a pattern, with substantial morphological differ- entiation between Up. citrata, Up. bakeriana and Up. korupensis, but a lack of support at subtending nodes. Uvariopsis korupensis is retrieved as paraphyletic and the two specimens sampled here (Couvreur 1039 and Louis 1863) come from different localities. They might belong to different isolated relictual popu- lations failing to coalesce due to the persistence of ancestral polymorphisms (Pennington and Lavin 2016). The species Up. bakeriana and Up. citrata likely emerged from two populations that diverged from the ancestral Up. korupensis population. This remains to be clarified with a denser sampling (in particular of Up. submontana) or with a phylogeographic and adapted population genomics approaches (Hardy et al. 2013; Migliore et al. 2019; Helmstetter et al. 2020a).
New and under collected species
In addition to the results discussed above, our sampling and analysis con- firmed the presence of new and/or under-collected species, which we detail here. Thanks to our dense sampling in the genus Uvariopsis, we were also able to test species limits, and concluded that several names are actually syn- onyms, which we detail under each concerned species in the Taxonomic treat- ment section below.
Morphologically, Uvariopsis sessiliflora stands out from the other Uvariopsis species by having sessile flowers and leaves less than 20 cm long (Up. citrata also has sessile flowers but leaves more than 30 cm long). The only known specimen representing this species is its type specimen (Mildbraed 52339), col- lected in 1911 in Lomié, a relatively well collected locality of Cameroon (Sonké and Couvreur 2014). This specimen is relatively poor in information as it has only has a small branch, one flower and one monocarp. Here we were able to sequence this specimen and it turns out that it is phylogenetically embedded within Up. dioica (Fig. 1, Suppl. materials 1, 2), indicating that Up. sessiliflora
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and Up. dioica are the same phylogenetic species. It seems that the specimen Mildbraed 5239 represents a rare extreme in the morphological variation of Ud. dioica, with severe reduction of the flower pedicel. This also explains why no similar specimen was collected after all this time in a such relatively well explored locality. We thus make it synonym under the name Up. dioica.
The recently described species Uvariopsis etugeana Dagallier & Couvreur (Couvreur et al. 2022), is a rare tree species only known from two localities in Cameroon. Our results confirm it is phylogenetically different from other Uvariopsis species (Fig. 1, Suppl. materials 1, 2).
Uvariopsis noldeae Exell & Mendonga is a species endemic to Angola (Exell and Mendonca 1951; Paiva 1966) and only known from the type specimen (Nolde 576). It is morphologically similar to Uvariopsis solheidii (De Wild.) Robyns & Ghesg., except for the young branches that are sparsely pubescent to glabrous whereas young branches of Up. solheidii are tomentose to short- ly tomentose suggesting the names might be synonymous. Our phylogenetic analyses, however, revealed with strong support that Up. no/deae is genetically different from Up. solheidii, being sister to Up. dioica and Up. congolana, with Up. solheidii forming a strongly supported monophyletic group (Fig. 1, Suppl. materials 1, 2).
Uvariopsis congensis differs from the other Uvariopsis species by its rela- tively small to medium sized leaves (less than 180 mm long), globose flower buds (vs. conical), and short flowering pedicels (less than 12 mm long). It is a widespread species distributed from Central Africa (Cameroon, Gabon) to East Africa (Uganda, Kenya) (Robyns and Ghesquiére 1933a; Verdcourt 1971a). In- terestingly, some of the specimens we identified as Up. congensis were from West Africa, (Sierra Leone to Ghana), thus outside of its suggested range. A thorough examination of these West African specimens revealed they differed by the morphology of their fruits. Moreover, our molecular phylogenetic analy- ses retrieved these West African specimens (referred as Uvariopsis oligocarpa on the Fig. 1 and Suppl. materials 1, 2) as monophyletic with strong support, and clearly separated from the Central and East African specimens (Fig. 1, Sup- pl. materials 1, 2). Sterile specimens of Up. oligocarpa are similar to Up. congen- sis and Dennettia tripetala, but are easily differentiated when female flowers or fruits are available. We thus describe these specimens under the new species Uvariopsis oligocarpa Dagallier & Couvreur.
Finally, the specimens of Uvariopsis congensis from East Africa (Verdcourt 1971a) are also morphologically different from the specimens distributed in Central Africa. The East African specimens represent trees from 7 to 15 meters tall (vs. shrubs to trees from 2 to 7 meters tall for the Central African speci- mens) and they have narrowly elliptic laminas with a length:width ratio between 3 and 4 (vs. elliptic to obovate with a length:width ratio comprised between 2.1 and 3.1). Interestingly, the morphological differences between the two morpho- types are not supported by our phylogenetic analyses (Fig. 1, Suppl. materials 1, 2). Thus given our sampling we shall refrain from splitting Up. congensis in two different species. However, to account for the morphological differences between the two morphotypes, we describe a new variety Uvariopsis congensis var. angustifolia Dagallier & Couvreur corresponding to the East African mor- photype (see Taxonomic Treatment below).
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Collection ATBP 666 (African Tropical Biodiversity Programme, M004937010) collected from the Budongo Forest Reserve in Uganda (as “Uvariopsis sp. nov. Uganda” in Fig. 1 and Suppl. materials 1, 2), is a sterile specimen tentative- ly identified as Up. congensis. Indeed, the leaves of this specimen resemble Up. congensis except for its longer petioles when compared to typical Up. con- gensis (ca. 6 mm vs. 2.5-5 mm in Up. congensis). Interestingly, our results recovered this specimen as sister to the clade formed by Up. lovettiana and Up. congensis, with strong support (Fig. 1, Suppl. materials 1, 2) and thus ge- netically very different from Up. congensis. This specimen could thus be an un- described species. Unfortunately, the available material is too poor for a proper species description. This species might be rare occurring only in the Budongo Forest Reserve. Plant surveys of this locality are relatively old (Synnott 1985) and it has recently been assessed as a key biodiversity area (Plumptre et al. 2019). Similarly, a specimen collected from Kigoma area in western Tanzania (Kyoto University Expedition (KUE) 1039, EA000009849), and referred to as “Uvariopsis sp. nov. Tanzania” (Fig. 1, Suppl. materials 1, 2), appears to be a new taxon. Morphologically, it is close to Up. lovettiana but differs in having lamina with rounded base (vs. acute to decurrent), and subsessile pubescent monocarps (vs. stipitate and glabrous). The sequenced specimen is recovered as sister to either Up. noldeae with strong support (Suppl. material 2) or to the group formed by Up. noldeae, Up. dioica and Up. congolana (Fig. 1, Suppl. ma- terial 1) with weak support. This uncertainty probably comes from the fact that the specimen has low overall sequencing statistics (22% of the total reference covered at at least 10x; mean depth 6.1x). This would also explain its long sustaining branch. Nevertheless, the specimen passed our quality thresholds and is included. Our results confirm that it is a new species, although its phy- logenetic placement remains uncertain. These new species emphasize once again the great diversity of the East African region, with locations (mainly forest remnants) containing numerous endemic species or genera (e.g. Scharff 1992; Couvreur et al. 2009; Gosline et al. 2019; Dagallier et al. 2021).
Uvariodendron
Morphologically, the genus Uvariodendron R.E.Fr. represents the typical Annon- aceae flower (van Heusden 1992) and does not stand out by any particular character (in contrast to Uvariopsis for example with its 2 sepals and general- ly 4 petals, see above). Species of this genus can be recognized, however, by the combination of the following characters: the flowers are generally large in size, bisexual, sessile or shortly pedicellate (generally less than 2 cm, but up to 6.5 cm in Ud. anisatum) with numerous bracts, 3 sepals and two whorls of 3 free and sub-equal petals. The flower bud is globose, and in bud, the petals of the outer whorl are valvate all along their margins, whereas the petals of the inner whorl are valvate only at the apex. The stamens are numerous (ca. 200 to 3000) and there are generally many carpels (5 to 160 in number). The mono- carps are sessile to shortly stipitate (with stipes up to 12 mm long). Based on our dense species sampling, the genus is retrieved as monophyletic with strong support (Fig. 1, Suppl. materials 1, 2). We discuss below some implications of our results at the taxonomic level.
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East African Uvariodendron’s: an endless source of botanical discoveries
East Africa is a region that harbours a great plant diversity, with several spe- cies being endemic or narrow endemics (Scharff 1992; Burgess et al. 1998, 2007; Couvreur et al. 2009; Gosline et al. 2019; Dagallier et al. 2021; Cheek et al. 2022). This pattern is known to be the result of the topographic heterogeneity of this region (Droissart et al. 2018; Guillocheau et al. 2018) that could promote both recent divergence and persistence of more anciently lineages through time (Fjeldsa and Lovett 1997; Rahbek et al. 2019; Dagallier et al. 2020).
Recently, we described three new Uvariodendron species from the East Af- rican coastal forests based on their morphology: Uvariodendron dzomboense Dagallier, W.R.Q. Luke & Couvreur, Uvariodendron mbagoi Dagallier & Couvreur, and Uvariodendron schmidtii W.R.Q. Luke, Dagallier & Couvreur (Dagallier et al. 2021). Here, our phylogenetic analyses retrieved these species as monophylet- ic, confirming their species status (Fig. 1, Suppl. materials 1, 2).
In addition to these recently described species, our results reveal another undescribed species. It is represented by four specimens sampled here that were previously identified as Uvariodendron kirkii. These specimens all come from a restricted area in the Kimboza Forest Reserve (Morogoro, Tanzania), and this species is thus described as Uvariodendron kimbozaense Dagallier & Couvreur. Phylogenetically, it is sister to Ud. kirkii although clearly divergent at the molecular level (Fig. 1, Suppl. materials 1, 2). Morphologically, it also resem- bles Ud. kirkii, but differs by having larger flowers and different leaf dimensions (see Fig. 3, Table 2 and Taxonomic Treatment). Although the Kimboza Forest Reserve covers just 4.05 km? of lowland rain forest, the description of yet an- other new tree species underlines once again the major biological importance of this forest for biodiversity conservation (Rodgers et al. 1983). To date, an unpublished check list (see http://www.mikepalmer.co.uk/woodyplantecol- ogy/tropical/Kimboza.html) reports that Kimboza harbors 18 strict endemic plant species, including the monotypic Annonaceae genus Mwasumbia (Cou- vreur et al. 2009) as well as many other trees such as Cola kimbozensis Cheek and C. quentinii Cheek (Cheek et al. 2007), Turraea kimbozensis Cheek (Cheek 1989) or Vitex morogoroensis Walsingham & S.Atkins. (Cheek et al. 2019). This suggests that Kimboza is “probably the richest site for forest limestone point endemic plant species in tropical Africa” (Cheek et al. 2007, 2019).
In the Flora Zambesiaca (Robson 1960) a potential new species of Uvario- dendron was documented without being named because of the scarcity of the material. It is only known from a single specimen (Mendonca 2558A) collected in 1944 in Mozambique. This specimen was sequenced here and it appears genetically distinct from the other Uvariodendron species, being sister to the group of several other East African species (Ud. gorgonis, Ud. schmidtii, Ud. dz- omboense and Ud. pycnophyllum) with strong support (see Uvariodendron mos- sambicense in Fig. 1 and Suppl. materials 1, 2). Our results thus confirm that this specimen represents a new species. Morphologically, it is very similar to Ud. dzomboense by the short leaves (less than 130 mm long), narrowly elliptic and acute to slightly decurrent laminas, and the globose, ca. 5 mm in diameter and sessile flower buds. It differs by the number of carpels (ca. 5 vs. 50-75 in Ud. dzomboense) (Table 3). The description from the Flora Zambesiaca was based on a sheet from LISC. Our examination of this species is based on a
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G
Figure 3. Morphological characters differentiating Uvariodendron kimbozaense Dagallier (A, C, E, G) and Uvariodendron kirkii Verdc. (B, D, F, H) A flowering pedicel with bracts and sepals, side view, note the imbricate sepals B flowering pedicel with bract scar and sepals C flower, with one outer petal and two inner petals gnawed, top view, note the slight transversal curvature of the inner petals D flower, top view, note the ‘boat-shaped’ inner petals E, F simplified representations of the flowers, from above, yellow marking highlights transversal curvature of the petals G, H Simplified representations of the transversal cut of the leaf, by the midrib. A, C Dagallier 49 (type) B, D Dagallier 23. Photos and drawings Léo-Paul Dagalli- er. Abbreviations: B, bract; brs bract scar; ca, carpel; ip, inner petal; lam, lamina; mlo, lower (abaxial) side of the midrib; mup, upper (adaxial) side of the midrib; op, outer petal; sep, sepal.
sheet from WAG that contains a single monocarp, thus slightly enhancing the initial description of the species (Robson 1960). The monocarp has a short stipe (ca. 12 mm long) which also differentiates it from Ud. dzomboense that has sessile monocarps. Even if the material remains scarce for a complete
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Table 2. Morphological comparison between Uvariodendron kimbozaense and Uvariodendron kirkii (see also Fig. 3). In bold: character unique to the species.
Lamina Midrib relief
Flower bud Bracts Sepals Petals size | Inner petals shape base above
Uvariodendron acute to slightly globose, 1 at base of the pedicel | 3-6.5mm long, 4-8 10-20 mm strongly kirkii decurrent impressed 1.3-6 mm and sometimes 1 on mm wide, very broadly | long,6-13 | transversally curved
(Fig. 3H) diameter the upper half of the to broadly ovate, mm wide (“boat-shape”)
pedicel (Fig. 3B) connivent (Fig. 3B) (Fig. 3D, F)
Uvariodendron acute to | slightly raised globose to | 1 at base of the pedicel | 6-12 mmlong,12-21 | 16-39 mm | slightly transversally kimbozaense rounded | withacentral | oblate,7-16 | and from 1 to 4 along mm wide, depressed long, 9-19 curved (Fig. 3C, E)
groove all mm diameter |__ the pedicel (Fig. 3A) ovate, imbricate mm wide
along (Fig. 3G) (Fig. 3A)
Table 3. Morphological comparison between Uvariodendron dzomboense and Uvariodendron mossambicense. In bold:
character unique to the species.
Lamina shape Lamina size Flower bud Carpels number Uvariodendron elliptic to narrowly elliptic, acute to slightly decurrent at base, | 65-132 mmlong, | globose, ca. 4.5 mm in 50 to 75 dzomboense attenuate at apex 20-45 mm wide diameter, pubescent Uvariodendron elliptic, acute to slightly decurrent at base, attenuate at apex | 80-135mmlong, | globose, ca. 6.5 mm in ca. 5 mossambicense 30-50 mm wide diameter, pubescent
description, we provide evidence from both phylogeny and morphology that this species is distinct from the other known Uvariodendron species. We thus name this species Uvariodendron mossambicense Robson ex Dagallier & Cou- vreur and provide a description as complete as possible (see the Taxonomic Treatment section).
East Africa has been relatively well explored botanically, as shown by the completion of the Flora of Tropical East Africa (Beentje 2015) and the publica- tion of several parts of the Flora Zambesiaca (Exell and Wild 1960). However, our descriptions of several new species suggest that other botanical discov- eries might arise from further exploration (Cheek et al. 2022). This stresses the importance of local botanical initiatives (e.g. Binggeli 2019; Bingham et al. 2021; Hyde et al. 2021).
The morphological continuum of Uvariodendron fuscum
In the Flora of Cameroon (Couvreur et al. 2022), the name Uvariodendron mi- rabile R.E.Fr. was synonymized under Uvariodendron fuscum (Benth.) R.E.Fr. Here we sequenced both the type (Preuss 1378) and paratype (Lehmbach 178) of the name Ud. mirabile, both specimens clustering with specimens identi- fied as Ud. fuscum (e.g. Mildbraed 6428, a paratype of the name Ud. fuscum) (Fig. 1, Suppl. materials 1, 2), confirming they are conspecific. Note that when described, Ud. occidentale was distinguished from Ud. fuscum (as Ud. mirabile) based on morphology (Le Thomas 1967). This holds up from a phylogenetic point of view as Ud. occidentale is clearly separated from Ud. fuscum (Fig. 1, Suppl. materials 1, 2).
Morphologically, Ud. fuscum (Benth.) R.E.Fr., Ud. giganteum (Engl.) R.E. Fr. and Ud. magnificum Verdc. share morphological similarities and differ- ences. They mainly diverge along a morphological continuum by the size of their leaves (lamina length) and the size of their flowers (sepals and petals
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600
400
200
200
150
100
50
Lamina length (mm)
© © RB av 00 ©
fusc.
Lamina width (mm)
0° PEes
fusc.
dimensions, number of carpels), with Ud. magnificum having larger leaves and flowers than Ud. giganteum, with the latter having larger leaves and flowers than Ud. fuscum (Fig. 4, Table 4). In addition, Ud. magnificum flowers have api- cally imbricate inner petals while the other Uvariodendron species have apically connate inner petals (Verdcourt 1969). In terms of similarities, they all present elliptic to obovate leaves. Uvariodendron fuscum and Ud. giganteum have simi- lar sepals (fused over up to half of their length), inner petals (free, obovate) and outer petals (free, ovate). Uvariodendron giganteum and Ud. magnificum have young branches covered with long and soft hairs producing a whitish appear- ance quickly falling off with age, whereas the young branches of Ud. fuscum vary from being sparsely pubescent to glabrous. Some of the characters that supposedly discriminate the species are overlapping (e.g. lamina length), par- ticularly concerning Ud. fuscum and Ud. giganteum.
Sepals length (mm) Sepals width (mm)
—s AK fo)
] 20 §] ‘J
fusc. gig. mag. fusc. gig. mag.
Outer petals length (mm) Outer petals width (mm)
I 60 ° 40 1 3 oo Yl
fusc. gig. mag. fusc. gig. mag.
we
oo @°
Carpels number Inner petals width (mm)
fo} 150 a
Inner petals length (mm)
. 40 , i 40 = 50 d a ma | a
mag. fusc. gig. mag. fusc. gig. mag. fusc. gig. mag.
Figure 4. Morphological continuum in Uvariodendron fuscum: traits comparison for var. fuscum (fusc.), var. giganteum (gig.) and var. magnificum (mag.). Each point represents a measurement. Vertical bars span the minimum and maximum values of the focal traits. Photos, left: leaf of Couvreur 1046; top right: flower, below view, of Couvreur 1046; below right: flower, top view, of Couvreur 990 (CC BY-NC 4.0 Thomas Couvreur).
Table 4. Uvariodendron fuscum: morphological comparison between var. fuscum, var. giganteum and var. magnificum. In bold: character useful to differentiate the varieties.
Ud. fuscum
var. fuscum
var. giganteum
var. magnificum
Young branches indumentum Lamina size Sepals size Petals size Carpels number sparsely pubescent to glabrous 160-450 mm long, 11-23 mm long, | 20-42 mm long, 20 to 70 43-118 mm wide 13-26 mm wide | 15-26 mm wide with long soft hairs producing a whitish 357-676 mm long, 20-30 mm long, | 21-40 mm long, 50 to 100 appearance quickly falling off 84-225 mm wide 16-26 mm wide | 17-30 mm wide with long soft hairs producing a whitish 210-750 mm long, 30-55 mm long, | 50-70 mm long, 150 to 160
appearance quickly falling off 57-215 (250) mm wide | 30-43 mm wide | 36-47 mm wide
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Phylogenetically, the specimens of the three species clustered together, with strong support at the crown node and a weak to moderate support at the internal nodes (Fig. 1, Suppl. materials 1, 2). The phylogenetic branches are short (Fig. 1, Suppl. material 2) indicating a low divergence between the specimens and both Ud. fuscum and Ud. giganteum are retrieved as para- phyletic. This suggests that gene flow is still occurring between popula- tions. We thus propose that the three described species are actually three different morphotypes of the same species. Uvariodendron fuscum rep- resents the smaller morphotype (small leaves and flowers relatively to the others), Ud. magnificum represents the greater morphotype (large leaves and flowers relatively to the others), and Ud. giganteum represents the in- termediate morphotype. The imbrication of inner petals of Ud. magnificum that Verdcourt (1969) described as a synapomorphy for the species should be considered as a developmental constraint imposed by the size of the pet- als. Indeed, in bud, we can imagine that the only way for such long (50-53 mm long) and wide (36-38 mm wide) petals to arrange with the other floral elements is to overlap.
The name Ud. giganteum was already reduced into synonymy with Ud. fus- cum in the Flora of Cameroon (Couvreur et al. 2022). Here we thus synonymize the name Ud. magnificum with Ud. fuscum. The first mention of Ud. fuscum dates back to 1862, as Uvaria fusca (Bentham 1862), whereas the name Ud. magnificum dates back to 1969 (Verdcourt 1969). Given the priority rule (Tur- land et al. 2018), the name Uvariodendron fuscum prevails. The description of the species is given in the Taxonomic Treatment section below.
The complexity of Uvariodendron molundense
The species Uvariodendron molundense (Engler & Diels) R.E.Fr. is distributed in Cameroon and Gabon. In 1969, Le Thomas synonymized the names Uvario- dendron mayumbense and Uvariodendron letestui with Ud. molundense. Indeed, the position of the flowers along the trunk and branches, previously used to discriminate these species (Fries 1930), was no longer valid as some spec- imens are both cauliflorous and ramiflorous (Le Thomas 1969). Le Thomas (1969) also described the variety Uvariodendron molundense var. citrata form some specimens from Gabon exhibiting a strong lemon scent. The examina- tion of 106 specimens identified as Ud. molundense revealed that this species shows a great morphological variability, especially for the leaf shape. For exam- ple, some specimens show young leaves with decurrent bases, whereas older leaves have a rounded base. The specimens identified as Ud. molundense form three phylogenetically supported groups separated by relatively high molecular divergence (Fig. 1, Suppl. materials 1, 2), at least as much molecular divergence as between other clearly morphologically divergent species (e.g. between Ud. dzombense and Ud. pycnophyllum). Although the three groups have morpho- logical similarities, we were able to distinguish them and we thus propose to separate them in three distinct species: Ud. molundense, Ud. citriodorum (Le Thomas) Dagallier & Couvreur, and Ud. pilosicarpum Dagallier & Couvreur. The full and valid descriptions of Ud. citriodorum and Ud. pilosicarpum are given in the Taxonomic Treatment section.
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Taxonomic revision of Dennettia, Uvariodendron and Uvariopsis Taxonomic history Uvariodendron
The names referring to species later placed within Uvariodendron were first de- scribed by Bentham (1862) as Uvaria connivens and Uvaria fusca and by Engler and Diels (1899) as Uvaria angustifolia and Uvaria gigantea (Engler and Diels 1899). The placement of these four tree species within the mainly liana genus Uvaria L. was based on similarities of the flowers. Based on this, Engler and Diels (1901) grouped them into the new section within Uvaria: sect. Uvariodendron Engl. & Diels (literally meaning “tree Uvaria’s”). For the next 30 years, several new tree species from Central and East Africa were described within this section: Uvaria megalantha Diels and Uvaria winkleri Diels (Diels 1907); Uvaria molunden- sis Diels and Uvaria pycnophylla Diels (Diels 1915); Uvaria letestui Pellegrin (Pel- legrin 1920); Uvaria gossweileri Exell and Uvaria mayumbensis Exell (Exell 1926) and finally Uvaria mannii Hutch. & Dalziel (Hutchinson and Dalziel 1927b).
In 1930, Fries (1930) revised several Annonaceae genera, and erected sect. Uvariodendron to genus status. The morphological characters that dis- tinguished Uvariodendron from the Uvaria L. were the tree habit (vs. liana in Uvaria), the indumentum of simple hairs (vs. generally stellate hairs) and flow- ers borne on the trunk or axillary (vs. terminal). Fries thus combined the “tree Uvaria” names cited above as: Uvariodendron angustifolium (Engl. & Diels) R.E. Fr., Uvariodendron connivens (Benth.) R.E.Fr., Uvariodendron fuscum (Benth.) R.E.Fr., Uvariodendron giganteum (Engl.) R.E.Fr., Uvariodendron letestui (Pel- legrin) R. E. FR., Uvariodendron mayumbense (Exell) R. E. Fr., Uvariodendron moludense (Diels) R. E. Fr. and Uvariodendron pycnophyllum (Diels) R. E. Fr. He also synonymised the name Uvaria megalantha Diels and Uvaria winkleri Diels with Uvariodendron connivens (Benth.) R.E.Fr., and described three new species: Uvariodendron calophyllum R.E.Fr., Uvariodendron mirabile R.E.Fr. and Uvariodendron usambarense R.E.Fr. (Fries 1930). A few years later, Exell and Mendonga combined the Angolan Uvaria gossweileri into Uvariodendron goss- weileri (Exell and Mendonga 1937). In 1955, Verdcourt published the new spe- cies Uvariodendron anisatum Verdc. from Kenya (Verdcourt 1955). Towards the end of the 1960's, several new species were described. Le Thomas described the new Uvariodendron occidentale Le Thomas distinguishing it from Uvario- dendron mirabile R.E.Fr. (Le Thomas 1967). In her Flore du Gabon, Le Thomas also described a new variety Uvariodendron molundense var. citrata Le Thomas, and synonymised the names Uvariodendron letestui Pellegrin and Uvarioden- dron mayumbense (Exell) R.E.Fr. with Uvariodendron molundense (Diels) R.E. Fr. (Le Thomas 1969). The same year, Verdcourt (1969) described three new species from East Africa: Uvariodendron gorgonis Verdc., Uvariodendron kirkii Verdc., and Uvariodendron magnificum Verdc. (Verdcourt 1969). Later, he also described Uvariodendron oligocarpum Verdc. (Verdcourt 1986), a species that was recently combined into Polyceratocarpus oligocarpus (Verdc.) Dagallier (Dagallier et al. 2021). Finally, Dagallier et al. (2021) published three new spe- cies from Kenyan and Tanzanian coastal forests: Uvariodendron dzomboense Dagallier, W.R.Q. Luke & Couvreur, Uvariodendron mbagoi Dagallier & Couvreur,
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and Uvariodendron schmidtii W.R.Q. Luke, Dagallier & Couvreur. In the Annon- aceae treatment for the Flora of Cameroon (Couvreur et al. 2022) the name Uvariodendron mirabile R.E.Fr. was synonymized with Uvariodendron fuscum (Benth.) R.E.Fr., as well as the name Uvariodendron giganteum (Engl.) R.E.Fr., that was combined into the variety Uvariodendron fuscum var. giganteum. Here, based on molecular and morphological analysis, we reassess the name Uvariodendron molundense into three species: Ud. molundense, Ud. citriodorum comb. et stat. nov. (ex. Ud. molundense var. citrata) and Ud. pilosicarpum sp. nov. and describe Ud. kimbozaense sp. nov. and Ud. mossambicense sp. nov. from East Africa. We also combine the name Ud. magnificum within Ud. fuscum as the variety Ud. fuscum var. magnificum comb. et stat. nov. Thus to date, and after this taxonomic work, Uvariodendron contains 18 species.
Note about the genus name Uva: According to Kuntze, who undertook no- menclatural work between the end of the 19" and the beginning of the 20" cen- turies, the generic name Uva should be used instead of Uvaria (Kuntze 1891). Indeed, Burman was the first to use the name Uva in his Thesaurus Zelanica (Burman 1736), but Linné changed the name to Uvaria while citing the same specimen and describing the same species (Linné 1747). Kuntze underlines that no nomenclatural rule precludes the use of the name Uva and favours its use over the name Uvaria (Kuntze 1891). Among other invalid Uvaria names, he corrects the names Uvaria gigantea Engler to Uva gigantea Engler, Uvaria an- gustifolia Engler & Diels to Uva angustifolia Engler & Diels (Kuntze 1891), Uvaria connivens Benth. to Uva connivens Benth. and Uvaria fusca Benth to Uva fusca Benth. (Kuntze 1903). Regardless, the use of Uva was apparently not followed by the scientific community even today as the name Uvaria continues to be used (Diels 1907; Meade and Parnell 2018; Turner 2018).
Dennetia and Uvariopsis
The genus Uvariopsis Engler was erected in 1899 with the description of Uvariopsis zenkeri Engler (Engler and Diels 1899). As circumscribed at the time, the genus was distinguished by its mainly unisexual flowers, two sepals and four fused petals. A few years later, Diels erected the genus Tetrastemma Diels with the description of Tetrastemma dioicum Diels (Diels 1907). Tetrastemma was also characterised by unisexual flowers with two sepals and four petals, but differed from Uvariopsis by being dioecious and cauliflorous (vs. monoe- cious and ramiflorous), and by having free petals (vs. fused at base). Based on the free petals character, four other Tetrastemma species were described in the following years: Tetrastemma solheidii De Wild. in 1909 (De Wildeman 1909), Tetrastemma pedunculosum Diels and Tetrastemma sessiliflorum Mild- br. & Diels in 1915 (Diels 1915), and Tetrastemma bakerianum Hutch. & Dalziel in 1927 (Hutchinson and Dalziel 1927a).
In parallel, two other genera, morphologically closed to Uvariopsis and Tet- rastemma were described: Thonnera De Wild. and Denettia Baker f. The genus Thonnera included a single species Thonnera congolana De Wild. differing from Tetrastemma by flowers having three petals (De Wildeman 1909). In 1953, how- ever, Fries combined this name into Uvariopsis as Uvariopsis congolana (De Wild.) R.E.Fr. without further justification (Fries 1953). The genus Denettia Bak- er f. was characterised by having bisexual flowers with three sepals and three
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petals, which differed from Tetrastemma, Thonnera, and Uvariopsis. It included a single species Denettia tripetala Baker f. (Baker 1913).
In 1933, Robyns & Ghesquiére described Uvariopsis vanderystii Robyns & Ghesq., and suggested it was a kind of intermediate species showing charac- ters of Tetrastemma, e.g. cauliflory, and of Uvariopsis, e.g. fused petals (Robyns and Ghesquiére 1933b). The same year, they revised the two genera with their ‘Essai de révision des genres Uvariopsis Engl. & Diels et Tetrastemma Diels (An- nonacées)’ (Robyns and Ghesquiére 1933a). In this publication, they described several new species: Uvariopsis batesii Robyns & Ghesq., Uvariopsis chevalieri Robyns & Ghesq. and Uvariopsis congensis Robyns & Ghesq. The later species is ramiflorous and has free petals, which again showed intermediate characters between Uvariopsis and Tetrastemma. Based on these intermediate species, Robyns & Ghesquiére (1933a) extended the morphological concept of Uvariop- sis and combined the name Tetrastemma with Uvariopsis. The new species combinations were: Uvariopsis bakeriana (Hutch. & Daltz.) Robyns & Ghesq,., Uvariopsis dioica (Diels) Robyns & Ghesq., Uvariopsis pedunculosa (Diels) Robyns & Ghesq., Uvariopsis sessiliflora (Mildb. & Diels) Robyns & Ghesg., Uvariopsis solheidii (De Wild.) Robyns & Ghesq. In 1948, Pellegrin described Uvariopsis letestui Pellegr., a species from Gabon (Pellegrin 1948), and three years later Exell and Mendonca described a species from Angola: Uvariopsis noldeae Exell & Mendonga (Exell and Mendonga 1951). In 1952, Keay published the species Uvariopsis globiflora Keay (Keay 1952). He also combined a spe- cies previously described by Chevalier under the name Uvaria spectabilis Chev. (Chevalier 1920) and cited in the Flora of Tropical West Africa as Uvaria spect- abilis Chev. ex Hutch. & Dalziel (Hutchinson and Dalziel 1927a) into Uvariopsis guineensis (Chev. ex Hutch. & Dalziel) Keay (Keay 1952). More than 30 years later, Verdcourt described Uvariopsis bisexualis Verdc. from Tanzania. Although this species has bisexual flowers, Verdcourt placed it in Uvariopsis based on pollen morphology closely ressembling species of Uvariopsis (Verdcourt 1986). The concept of Uvariopsis was thus enlarged to include bisexual species.
Gereau and Kenfack (2000) described the species Uvariopsis korupensis Gereau & Kenfack followed by the publication of Uvariopsis submontana Kenfack, Gosline & Gereau (Kenfack et al. 2003). In that later publication, the name Denettia tripetala Baker f. was combined into Uvariopsis tripetala (Baker f.) G.E. Schatz. based on the concept of Uvariopsis now also included species with bisexual flowers (Verdcourt 1986; Kenfack et al. 2003). More recently, the Tanzanian species Uvariopsis lovettiana Couvreur & W.R.Q. Luke (Couvreur and Luke 2010) and the Gabonese species Uvariopsis citrata Couvreur & Niangadouma (Couvreur and Niangadouma 2016) were described. Inthe Flora of Cameroon Annonaceae (Couvreur et al. 2022), the species Uvariopsis etugeana Dagallier & Couvreur was described and the name Uvariopsis vanderystii Robyns & Ghesg. was synonymized with Uvariopsis pedunculosa (Diels) Robyns & Ghesgq. Finally, the species Uvariopsis dicaprio Cheek & Gosline was described from Cameroon (Gosline et al. 2022). In the present work, based on molecular and morphological analyses, we retain the name Dennettia tripetala and thus the genus Dennettia (see discussion above). We also describe a new species, Up. oligocarpa sp. nov., and synonymize the names Up. sessiliflora with Up. dioica, Up. globiflora with Up. guineensis and Up. letestui with Up. solheidii. For the two laters, we combine the names into varieties as Up. guineensis var.
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globiflora comb. et stat. nov. and Up. solheidii var. letestui comb. et stat. nov., respectively. We also describe a new variety of Up. congensis, Up. congensis var. angustifolia var. nov. and provide a preliminary description of potentially three new species which lack sufficient material to be formally described. This brings the total number of Uvariopsis species to 17 (and three that have yet to be formally described).
Morphology and informative characters Vegetative characters
The genera Dennettia, Uvariodendron and Uvariopsis are trees or shrubs with plagiotropic branches on an orthotropic axis, with indumentum of simple hairs and with no latex or exudate. A distichous phyllotaxis of the primary axis (the trunk) was reported for Ud. pycnophyllum (Johnson 2003) but no information was reported for the other species nor for Dennettia and Uvariopsis. The trunks are generally cylindrical and straight, with no buttresses. The base of the trunk of some Uvariopsis species (Up. dioica, Up. submonana, Up. korupensis) can be thickened by the growth of numerous inflorescences clumped on the trunk between the ground to generally ca. 50 cm (up to 4 m).
The branches can be sparsely pubescent when young, but the hairs generally fall off with age. The dense brown tomentum on the young branches persist- ing on older branches distinguishes Ud. calophyllum from the other species of Uvariodendron. The species Ud. fuscum (var. giganteum and var. magnificum) also have a characteristic indumentum of long soft hairs producing a whitish ap- pearance on the younger branches, but that quickly disappear in older branches.
In the three genera, the leaves are distichous, simple, entire, exstipulate, with the midrib impressed above, raised below, the secondary veins weakly brochi- dodromous to brochidodromous and the tertiary veins reticulate. Dennettia has relatively small (less than 160 mm long) elliptic leaves, while Uvariodendron and Uvariopsis have a range of leaf shapes, from elliptic to obovate to oblong, ranging from 65 to 750 mm long. Uvariodendron fuscum var. giganteum has one of the longest leaves of Annonaceae in Africa, up to 60 cm long (Couvreur et al. 2022). In contrast to other genera (e.g. Uvariastrum; Couvreur 2014) the leaf base shape is not a very useful taxonomic character to distinguish species because several different shapes (e.g. from acute to rounded) can occur within species. However, subcordate leaf bases are generally found in Up. bakeriana, Up. citrata, Up. korupensis, and Up. submontana, and decurrent leaf bases in Ud. pilosicarpum, Up. bisexualis, Up. congensis, Up. lovettiana, Up. oligocarpa and Up. zenkeri. Some species have apparent complex leaf bases, like rounded in shape but minutely decurrent when looking at the very base (Ud. citriodorum, Ud. gorgonis, Ud. molundense). In Uvariodendron kimbozaense, the midrib is slightly raised above with a central groove all along the length of the midrib. This is unique in the genus, but raised midribs occur in other genera such as Isolona, Monodora and Ophrypetalum (Couvreur 2009), and raised and grooved midribs occur in Cremastosperma (Pirie et al. 2018). The petiole in Uvariopsis is generally short and thick, less than 6 mm long with a length:width ratio less than 2, whereas in Uvariodendron the petiole is generally longer than 4 mm with a length:width ratio between 2 and 5.
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In Uvariodendron, several species (Ud. dzomboense, Ud. gorgonis, Ud. mos- sambicense and Ud. schmidtii) show ‘eragrostiform’ leaf buds, that are terminal or axillary buds composed of several (generally 5 to 12) distichous and densely pubescent scales (Figs 25A, 36C, 44B). The term ‘eragrostiform’ relates to the genus Eragrostis (Poaceae) and its typical form of flattened spikelet composed of compact and clustered florets. Even though this feature is striking, it should be noted that not all the specimens of a same species present this kind of buds, so it is hard to use it as a diagnostic character. The phenology or the en- vironment may influence the establishment of eragrostiform buds, which might protect the meristem against drought or herbivores.
The scent of crushed leaves and/or bark can be used as a distinctive char- acter. Uvariodendron citriodorum and Up. citrata emit a strong lemon scent (Le Thomas 1969; Couvreur and Niangadouma 2016), a feature also shared by some specimens of Ud. gorgonis. Crushed leaves and bark of Ud. mbagoi have a strong bergamot scent (between orange and lemon) (Dagallier et al. 2021), and all parts of Ud. anisatum smell of anise. Ud. angustifolium is also reported as having a strong aromatic scent.
Inflorescences and flowers
In contrast to sterile parts, Dennettia, Uvariodendron and Uvariopsis have very different fertile parts. In Annonaceae, the inflorescence is a rhipidium, i.e. deter- minate (sympodial) inflorescence with a terminal flower and lateral cymose and monochasial partial inflorescences (Weberling and Hoppe 1996). Inflorescences of Dennettia, Uvariodendron and Uvariopsis are axillary and borne on leafy twigs or borne on old branches (ramiflory) or on the trunk (cauliflory), depending on the species. The position of the flower was regarded as an important charac- ter to characterize some species like Ud. molundense and Up. guineensis (Keay 1952; Le Thomas 1967, 1969) but it appears to be unreliable in Uvariodendron and Uvariopsis (see also Le Thomas 1969). In the three genera, the flower pedicels are not articulate and display from one to six bracts at their base and from one to four bracts on the lower half of the pedicel. As flowers mature, most of the bracts fall off, except the uppermost bract. Usually, fallen bracts leave a scar on the pedicel.
In Dennettia, the inflorescences are axillary and borne on leafy twigs or borne on old branches, held by a tiny peduncle. They can be composed of up to six flowers, but one or two-flowered inflorescence are the most common. The flow- ers of Dennettia are bisexual. They are composed of one whorl of three sepals and one single whorl of three petals, which is characteristic of the genus in the Monodoreae. In Annonaceae, single whorls of three petals can be found in An- nickia, Annona, and Dasymaschalon (van Heusden 1992).
In Uvariodendron, the inflorescences are axillary and borne on leafy twigs, borne on old branches or borne on the trunk. The axis of the inflorescences are contracted, rendering their interpretation difficult without a detailed morpho-an- atomical study. They appear to be rhipidia composed of one or two (in most species), three (Ud. calophyllum, Ud. gorgonis, Ud. mbagoi) or rarely up to 11 (Ud. kimbozaense) flowers. Generally, in multi-flowered rhipidia, the flower in the terminal position is fully developed while the lower flowers on the axis are buds.
Flowers in Uvariodendron are bisexual with one whorl of three sepals and two whorls of three petals, as usually found in Annonaceae (van Heusden 1992). The
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fusion and arrangement of the sepals is used to distinguish between species: al- ways fused (Ud. angustifolium, Ud. dzomboense, Ud. fuscum, Ud. mossambicense, Ud. occidentale, Ud. pycnophyllum, Ud. schmidtii), always imbricate (Ud. citriodo- rum, Ud. kimbozaense, Ud. mbagoi, Ud. pilosicarpum), or from free to fused to im- bricate (Ud. anisatum, Ud. calophyllum, Ud. connivens, Ud. gorgonis, Ud. kirkii, Ud. molundense). The sepals are smaller and morphologically different to the petals. The outer and inner petals are subequal in length, ranging from 10 to 70 mm at an- thesis. In bud, the outer petals are valvate (adpressed against each other all along the margin) whereas inner petals are valvate only at the apex. In mature flowers, the outer and inner petals are free, but the inner petals can remain adpressed at apex. In most species, the petals are cream to yellow in color, with a red/purple marking at the base of the inner side. Uvariodendron connivens has petals that are pink to red all over and on both sides at anthesis, while the outer petals of Ud. calophyllum are covered with a dense tomentum leading to a brown flower. The stamens are numerous (more than 200), with linear anthers and truncate apical prolongation of the connective. The carpels vary from five to 160, they are free, lin- ear, with a coiled stigma. The monocarps are sessile or subsessile and cylindrical.
Uvariopsis has inflorescences borne on trunk in most of the species, but can be axilary to leaves on young branches (Up. congensis, Up. guineensis, Up. lovettiana, Up. oligocarpa, Up. zenkeri). They are generally composed of one to three flowers. Like in Uvariodendron, the peduncle and partial peduncle are contracted, rendering their interpretation as rhipidium difficult. In particular, Up. dioica, Up. submontana and Up. korupensis have inflorescences in clumps of up to 50 flowers on the trunk.
The flower buds of Uvariopsis have different shapes important to discrimi- nate between species (Kenfack et al. 2003). They can be globose (Up. congen- sis, Up. guineensis, Up. lovettiana, Up. oligocarpa, Up. pedunculosa, Up. zenkeri), ovoid to conical (Up. bisexualis, Up. citrata, Up. dioica, Up. noldeaea Up. sol- heidii, Up. submontana), pyramidal (Up. congolana, Up. dicaprio, Up. etugeana), or narrowly and long conical (Up. bakeriana, Up. korupensis). Flowering pedi- cels in Uvariopsis varies greatly from less than 11 mm (Up. bakeriana, Up. ci- trata, Up. congensis, Up. etugeana, Up. oligocarpa, and Up. zenkeri) to more than 100 mm up to 400 mm (Up. congolana, Up. pedunculosa). The flowers of Uvariopsis have one whorl of two sepals and one whorl of four petals (except Up. congolana which has three petals). In Annonaceae, flowers with two sepals and four petals are rare and can be found in only a few other genera such as Disepalum or Tridimeris (van Heusden 1992). The petals are usually free, but can be fused in some species (Up. congolana, Up. guineensis, Up. korupensis, Up. pedunculosa, Up. submontana, and Up. zenkeri). Another rare character in Annonaceae exhibited by Uvariopsis is its exclusively unisexual flowers (except for Up. bisexualis that has bisexual flowers). In Annonaceae, unisexual flow- ers are found in several androdioecious species, e.g. in Polyceratocarpus (Cou- vreur et al. 2009), Diclinanona (Erkens et al. 2014), Ephedranthus (Lopes et al. 2014) , Pseudephedranthus (Erkens et al. 2017), Klarobelia or Pseudomalmea (Lopes et al. 2018). Species with exclusively unisexual male and female flow- ers are rarer and found only in a few species within genera such as Anonidium, Monanthotaxis, Pseuduvaria, Stelechocarpus and Winitia (van Heusden 1992; Chaowasku et al. 2013; Hoekstra et al. 2021; Couvreur et al. 2022). Unisexual Uvariopsis species are monoecious, i.e. male and female flowers on the same
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individual, even in the species Up. dioica that has a misleading specific epithet. The number of stamens varies from 100 to 900, with anthers linear and connec- tive prolongation truncate or absent. The number of carpels varies from three to 280; they are free, linear, with a coiled, truncate or globose stigma.
The fruits of Uvariopsis are composed of several sessile to subsessile mono- carps generally cylindrical in shape. Their texture and pubescence can be informa- tive: either smooth and not ridged (Up. congensis, Up. dioica, Up. guineensis, Up. korpensis, Up. lovettiana, Up. oligocarpa) or wrinkled to verrucose (Up. bakeriana, Up. congolana, Up. pedunculosa, Up. solheidii), and either pubescent to tomentose (Up. pedunculosa, Up. oligocarpa, Up. zenkeri) or sparsely pubescent to glabrous.
Pollination and seed dispersal
The pollination biology of Dennettia, Uvariodendron and Uvariopsis is poorly known for most of the species, except for Ud. connivens, Ud. calophyllum, Up. bakeri- ana and Up. pedunculosa (Gottsberger et al. 2011; the specimen identified as Up. congolana in this reference is actually Up. pedunculosa), and also Up. dioica (Mertens et al. 2018). Uvariodendron are mainly pollinated by beetles (Coleoptera, Scarabaeidae and Curculionidae). The inner petals remain connate at the apex until anthesis, forming a semi-closed pollination chamber in which the pollinators feed on pollen and mate (e.g. Figs 19G, 24F). The pollinators are attracted by the scent emitted by the flowers. Flowers of Ud. connivens and Ud. calophyllum were found to be thermogenetic, which could enhance the scent diffusion and the polli- nator attraction (Gottsberger et al. 2011). However, rather than active thermogen- esis, it is possible that the pollination chamber buffers the air temperature from outside. The petals of Uvariodendron flowers are thick and the pollinators feed on the petals and deposit their eggs in the petal tissue, which is testified by the gnaw marks on the petals (e.g. Fig. 29J), similarly to other Annonaceae species having thick petals (Gottsberger and Webber 2018). Although this probably doesn't play a role in pollination, we have seen completely eaten petals on flowers of Ud. kim- bozaense (Fig. 27D), with animal hairs stuck on the stigma exudate (Fig. 27G), suggesting that small mammals like rodents may feed on the petals. Direct ob- servation of such feeding on petals should, however, confirm this hypothesis.
In Uvariopsis, the species Up. bakeriana and Up. pedunculosa have been re- ported as emitting a strong pungent scent, and to be pollinated by flies (Dip- tera) (Gottsberger et al. 2011). Up. dioica has been reported to be pollinated by flies, cockroaches and orthopterans (Mertens et al. 2018), and pictures of living specimens of Up. dioica (Bidault 1558) and Up. guineensis (Bidault 4798) show flies visiting the flowers (e.g. Fig. 61F). Petals of Up. bakeriana are dark red to dark pink and verrucose, which looks like body flesh. This is characteristic of the sapromiophylous pollination syndrome (Gottsberger et al. 2011). Most of the Uvariopsis species present petals with flesh-like colors and texture. This suggests that sapromiophyly is the dominant pollination syndrome in Uvariop- sis. In contrast, the species Up. dicaprio present pale yellow-green flowers, Sug- gesting nocturnal pollinators such as moths (Gosline et al. 2022).
Similarly to pollination biology, data on seed and fruit dispersal of Dennettia, Uvariodendron and Uvariopsis remain scarce. Fruits of Uvariodendron are part of Western gorillas (Gorilla gorilla)’s diet (Rogers et al. 2004), as well as fruits of Up. congolana (Yamagiwa et al. 1994) and Up. solheidii (notes of specimen
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Fay 8384). Fruits of Up. solheidii are also eaten by small rodents and squir- rels (Gautier-Hion et al. 1985). Chimpanzees (Pan) and guenons (Cercopithe- cus) consume the fruits of Up. congensis (Lambert 2011; Watts et al. 2012; Kagoro-Rugunda and Hashimoto 2015).
Ethnobotany
Uvariodendron and Uvariopsis species are used for food. The ripe fruits of Ud. an- gustifolium (Jones 3480) and Ud. fuscum (van Andel 3761) are eaten, as well as the young leaves of Ud. connivens (Cheek 5180) and Ud. fuscum (Cheek 5145) that are boiled and used in soup. The bark of Ud. mbagoi (Dagallier 39) is used as infusion for tea or as spice in meat meals. The leaves of Up. citrata (Letouzey 9017) are used to wrap the fish during the cooking to give it an aromatic taste.
Uvariodendron and Uvariopsis species are also part of the pharmacopoeia of several local communities, such as in Benin and Cameroon where Ud. angusti- folium, Ud. connivens, Ud. fuscum, Up. bakeriana, Up. dioica and Up. korupensis are used to cure various conditions (Jiofack et al. 2009; Bele et al. 2011; Bada Amouzoun et al. 2019) or in Kenya where Ud. kirkii is used as contraceptive (Kaingu et al. 2017).
The fruits of Dennettia tripetala, also known as “pepper fruit”, are famous in West Africa for their spicy taste, especially in Nigeria (Fig. 51). The species is traditionally used for the anti-rheumatic, stimulant, antioxidant, antimicrobial and analgesic effects of its leaves, fruits, seeds, roots and stems (Aiyeloja and Bello 2006; Ajibesin et al. 2008; Iseghohi 2015; Rafiu and Sonibare 2016; Ola- tokunbo et al. 2018; Omage et al. 2019; Muhammed et al. 2021).
Other usages such as firewood and craft were reported for Ud. angustifolium, Up. bakeriana, Up. dioica, and Up. korupensis (Bele et al. 2011; Bada Amouzoun et al. 2019), as well as dye with fruits of Ud. connivens (Mbani 14).
Taxonomic treatment Ophrypetaleae
Ophrypetaleae Dagallier & Couvreur, trib. nov. urn:lsid:ipni.org:names:77326966-1
Type. Ophrypetalum Diels.
Description. Shrubs to trees; indument of simple hairs. Carpels 1-15. Mono- carps 1-10, sessile to shortly stipitate, 5 cm long or more, narrowly cylindrical, length:width ratio more than 5.
Included genera. Ophrypetalum Diels (1 species), Sanrafaelia Verdc. (1 species).
Key to the genera of Monodoreae as recognized in this study
1 Midrib of leaf blade clearly raised above; one single large fruit with seeds UOC E SG. dt ce cahaditvis cuctatt 1eaadsery deans Utceweshusiit es thud tame egandatienonscsd Mewes ghedons susvie ante 2 - Midrib of leaf blade impressed above, or slightly raised with a central groove all along the midrib above; fruits with distinct monocarps with uni- GrDrSSMAtC SCCOS A. Ah y .ccnsicrh lle ccmeamsbbed ue bacrahti lets, uananbecd Me rebates 3
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2 Corolla lobes similar and equal in length, forming a distinct tube at the base, margins generally Straight ...............ccccccssccecssseecesseeecsesseeesenees Isolona - Corolla lobes clearly differentiated into inner and outer petals (but basally fused); the outer ones longer than inner ones, margins generally undulated
DIMEN SIC scum te Pet en ctr tie Rt ysecer tant Rut Anus eet Pe oh ene nA Monodora 3 Sepals 2 and at least one of: petals 4, flowers unisexual........... Uvariopsis - Sepals 3 and petals 3 or 6 and flowers biSexUal...............ccccceeesceessseeeeeees 4 As “-Se@Pals sane tal Sd 2 ec pecs Be ere tet toe tok eee atten ere cee eeeettcee ace nee Meera ok 5 == MSCOalS: Sx Del alS:O wre kctesecs deuce duensss, oi see teen inst etes Son tote ynett crane dtnctee ine teseney ss 6
5 Calyx forming a short and thick receptacular tube (East Africa)....... Lukea - Calyx forming a ring with 3 lobes generally distinct (West Central Africa)....
Sea aa A ceeat eee RAE Re teeerenenrorenen: Reeesetee reese MEE Dennettia 6") -Petalseused ALDaS es .2.8 satel eter ek eee Marek ee emtedtnrere an umaleaeanee 7 AD PIRCRAIS. TCS es cies c csunerssscuee sat ca negiurnoapesttnn ppbunirtesimnnees caaseahtnaesaulbiunessbeanhrsesiuaee ats 8 7 Petals plicate, transversely folded in bud ............c eee eeeeeereeees Hexalobus - Petals not plicate, not folded in DUd..........0..... cc csseccessseeeeeee Asteranthe 8 Petals in a single whorl, calyx forming a thick receptacular tube................
Bae cddataitin seca rates eae Oa ah aati MR an eth cde eos shee cat seen Gea Monocyclanthus - Petals in two distinct whorls, calyx not forming a receptacular tube........ 9 9 Receptacle columnar; anther connective reduced to a tuft of hairs............
Be adie oa at ees Sea ROMe A eke wir data a rare feat eastern Bun cries aces ame Rama Raises Mischogyne - Receptacle convex to flat but not columnar; connective not reduced to a
TUPEOT IGS: <2 ces, fetes Perc Be erty rabeciie iede Sie anaes r dusts ates dea mre 10 10 Sepals reduplicate-valvate (ridged) in bud ............ cece eeeees Uvariastrum - Sepals not reduplicate-valvate (not ridged) in bud............... Uvariodendron
Dennettia Baker f., Cat. Pl. Oban 5 (1913) Figs 5, 6
Dennettia tripetala Baker f., Cat. Pl. Oban 5 (1913).
= Uvariopsis tripetala (Baker f.) G.E.Schatz, Novon 13(4): 447 (2003). Type. NIGERIA — Edo State * R.E. Dennett 44 (lectotype: K! (K000040959), desig- nated by Kenfack et al (2003), sheet designated by Couvreur et al (2022); isolectotype: K! (KO00040961)), Benin City; 6°20'N, 5°38'E; 01 Jan. 1907.
Description. Shrub to tree 1-5 m tall, D.B.H unknown; young branches sparsely pubescent to glabrous, old branches glabrous. Petiole 2-5 mm long, 1-1.5 mm wide, glabrous. Leaf lamina 72-155 mm long, 30-68 mm wide, length:width ra- tio 1.9-3.25, elliptic, papyraceous to coriaceous, base acute to decurrent, apex attenuate, acumen 6-13 mm long, surface above glabrous, surface below gla- brous; midrib impressed above, raised below, glabrous above, glabrous below; secondary veins 5-10 pairs, brochidodromous to weakly brochidodromous, slightly raised above, raised below; tertiary veins reticulate. Flowers bisexual. Flower buds globose. Inflorescences borne on branches or axilary, composed of 1 to 6 flowers. Peduncle ca. 0-1 mm long, ca. 1 mm in diameter. Flower ped- icel 3.5-10 mm long, 1-2.5 mm in diameter, pubescent to sparsely pubescent. Bracts 1 to 3 at base, upper bract 0.5-2 mm long, 1.5-2 mm wide, broadly ovate, pubescent outside, glabrous inside. Sepals 3, 1-3 mm long, 1.5-4 mm
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 37
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Figure 5. Dennettia tripetala Baker f A flowering branch B flower, one petal removed, showing receptacle C receptacle with stamens and stigmas D stamen, front view E carpel, front view F carpel, longitudinal section showing ovules G flow- er, top view H flower, side view I fruits collected for local use in Nigeria A-F material of drawings unknown, author of drawing unknown, modified from Baker (1913; plate 2) G Aké Assi 9543 H Jongkind 4356 I material unknown. Photos G, H Léo-Paul Dagallier | World Agroforestry (https://flic.kr/p/pZycpY).
wide, broadly ovate, fused up to more than 50% of their length, forming a per- sistent ring with the 3 lobes generally clearly distinct, curved downward on fruit pedicel, pubescent outside, glabrous inside, color unknown. Petals 3, 5-14 mm long, 4.5-10 mm wide, length:width ratio 1-1.7, broadly ovate to ovate, con- nivent in bud, free at anthesis, pubescent to sparsely pubescent outside, gla- brate inside, light brown to dark red outside, purplish pink inside. Stamens number unknown, 0.5-1 mm long, 0.3-0.5 mm wide, anthers linear, connective prolongation truncate. Carpels 8-30, 2-4.5 mm long, 0.5-2 mm wide, pubes- cent, free; stigma 0.5-1 mm long, 0.5-1 mm wide, coiled, pubescent. Fruiting
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 38
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Latitude
10°N
Ol O Pe
Oo
50S
bl pee =, —s. q ® O f ?) @ Dennettia tripetala 100W 5oW Oc BoE
Longitude
Figure 6. Distribution map of Dennettia tripetala. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
pedicel 5-14 mm long, 1-2.5 mm in diameter, pubescent to glabrous. Mono- carps, 1-7, 11-32 mm long, 5-18 mm wide, length:width ratio 1.5-2.3, cylin- drical, slightly constricted between the seeds when dried, sparsely pubescent to glabrous, greyish green when unripe to pink-reddish when ripe, subsessile; stipe 0.1-3 mm long, 1-2 mm wide, pubescent. Seeds 4-12 per monocarp, biseriate, 7.5-10 mm long, 2-5 mm wide, ellipsoid.
Distribution. Element of the Upper Guinean Domain and Lower Guinean Do- main of the Guineo-Congolian Region: Guinea, Sierra Leone, Ivory Coast, Ghana, Benin, Nigeria, Cameroon.
Habitat and ecology. Lowland mature or secondary rain forests, in west Af- rica reported from drier forests on rocky outcrops (Hawthorne and Jongkind 2006). Altitude: 250-975 ma.s.l.
Phenology. Flowers collected from February to April. Fruits collected from January to July.
Vernacular names. Cameroon: ‘Bushpépé’ (Westphal 9932). Ivory Coast: ‘Mi- chiti a petites feuilles’ (Aubréville 145). Nigeria: ‘Mmimmi’ in Igbo, ‘Ata Igebere’ or ‘Igberi’ in Yoruba, ‘Opipi’ in Idoma, ‘Imako’ in Urhobo, ‘Ako’ in Bini and Edo, ‘Nkarika’ in Efik and Ibibio (Aiyeloja and Bello 2006; Ajibesin et al. 2008; Rafiu and Sonibare 2016; Omage et al. 2019; Muhammed et al. 2021).
Uses. Fruits used as spice and leaves, roots, fruits and seeds used as lo- cal medicine.
Notes. This species resembles Uvariopsis congensis, Up. oligocarpa and Up. zen- keri in having elliptic leaves generally less than 16 cm long with decurrent base, but it clearly differs by its bisexual flowers having three sepals and three petals.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 39
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Preliminary conservation status. This species is distributed from Guinea to Cameroon. Its EOO is estimated at 705,671 km? and its AOO at 120 km7. Follow- ing IUCN criterion B, it would thus be assigned a status of LC.
Additional specimens examined. BENIN — Mono ° J.-P. Essou 1443 (BENIN, MO, WAG); Aplahoué, Kpédjihoundéhoué; 7°21'N, 1°44'E; 17 Feb. 1999 — Ouémé * A. Ako@gninou 2201 (BENIN, WAG); Kétou, Ewe; 7°28'N, 2°35'E; 01 Feb. 1999 - Zou — K. Kiippers 2059 (FR, WAG), Noyau Central forét class.Lama; 6°57'N, 2°07'E; 28 Feb. 1998. CAMEROON — South-West Region * D.W. Thomas 5661 (K, MO, P WAG), Nganjo. West bank of Meme River on Kumba Mbonge road; 4°33'N, 9°24'E; alt. 50 m; 25 Feb. 1986 « E. Westphal 9932 (WAG), Victoria; 4°01'N, 9°12'E; 04 Apr. 1978 « G.W.J. Mildbraed 10515 (K), Likomba — Pflangzung, 15-35 km NE of Victoria; 4°06'N, 9°20'E; alt. 50 m; 18 Oct. 1928 « T.D. Maitland 626 (K); Fako, Victoria (= Limbe), Bonjongo; 4°06'N, 9°08'E; alt. 600 m; Apr. 1929 « T.D. Maitland 627 (P), Victoria (= Limbe), Bonjongo; 4°06'N, 9°08'E; 1929 « T.D. Maitland s.n (K), Mt Cameroon; 4°15'N, 9°13’E; alt. 920 m; 1930 « T.D. Maitland s.n.14 (K), Mt Cameroon, Buea area; 4°12'N, 9°11'E; alt. 975 m; 1930. GHANA — Ashanti Region * J.K. Morton A3394 (K), Nyinahin range, W of Kunasi; 6°36'N, 2°07'W; alt. 700 m; 07 Jun. 1958 — Central Region * J.B. Hall GC43611 (K, WAG), Ojobi near Awutu; 5°29'N, 0°32'E; 29 Feb. 1972 * J.K. Morton s.n (K), About 1 mile N of Ojubi, Senya Beraku; 5°23'N, 0°29'E; 24 May. 1953 —- Unknown mgjor area * J.B. Hall GC43276 (K), Yaugwu F.R; alt. 460 m; 19 Mar. 1972. GUINEA — Kindia » D. Molmou 603 (P), Layah, Sousoude. Just avant Tonkoyah; 9°43'39.3"N, 13°12'26.6'W; alt. 12 m; 06 Jul. 2013. lvoRY CoAsT — Bouaflé + C.C.H. Jongkind 4356 (MO, WAG), Parc National de la Marahoue. Near south border; 6°59'N, 6°10'W; alt. 250 m; 11 Feb. 1998 — Bouaké « L. Aké Assi 18031 (G), Forét de Bamoro; 7°48'N, 5°05'W; 07 Jun. 1989 — Bouna = C. Geerling 2222 (K, WAG), Iringou (Gawi-Bania conf. Bamago); 8°58'N, 3°39'W; 15 Mar. 1968 + PP. Poilecot 1224 (G), RN. Comoé Sud; 8°45'N, 3°35'W; 13 Apr. 1986 « PP. Poilecot 4164 (G, MO), RN. Comoé Sud; 8°45'N, 3°35'W; 13 Apr. 1986 — Danané « A.J.M. Leeuwenberg 2999 (K, L, MO, P WAG), 2 km E of Danané; 7°16'N, 8°07'W; alt. 410 m; 06 Mar. 1959 - Oumé - A. Le Thomas 27 (P), Lamto-Station, Fleuve Bandama; 6°13'N, 5°01'30"W; 07 Jul. 1985 * A. Le Thomas 97 (P), Lamto-Station, Bandama; 6°13'N, 5°01'30"W; 26 Jul. 1985 — Sassandra « A. Aubréville 1957/163 (BR, K, P); 4°59'N, 6°08'W; 07 Mar. 1957 — Soubré « L. Aké Assi 9490 (G, P), Foret du Bassin de la Lobo; 6°07'N, 6°48'W; 22 Feb. 1967 — Vavoua « F.N. Kouamé 1470 (CSRS, G), F.C. du Haut-Sas- sandra, Centre. forét tres dégradée, relevé FNK20; 7°07'N, 7°00'W; 07 Apr. 1995 — Unknown major area * A. Aubréville 145 (K, P); 7°37'26.4'N, 5°33'14.4"W; 28 Feb. 1957 « L. Aké Assi 13255 (G), Mont Niénokoué; 5°23'N, 7°10'W; 19 Jan. 1976 * L. Aké Assi 9543 (G, K, P), Mt Mafa; 5°52'N, 4°04'W; 14 Mar. 1967. NI- GERIA — Anambra State » J.C. Okafor FHI35869 (K), Onitsha; Nnwei; Ukpor — Nzagha village; 6°50'N, 6°50'E; 22 Oct. 1956 — Cross River State * C.F.A. Onochie FHI36331 (K), Calabar, Ikot Efanga, c. 12 miles from Calabar on the Oban road; 4°58'N, 8°29'E; 09 Feb. 1957 — Oyo State + C.E. Darter 41837 (K), Olokemeji For- est Reservee; agbola pool, Ogun River; 7°25'N, 3°32'E; 06 Apr. 1958 — Unknown major area * J.O. Ariwaodo ARS1184 (K), Munta Village. SIERRA LEONE — West- ern Area * J.K. Morton SL2013 (FHI, IFAN, K, SL, WAG); Western Area, near York by Whale Bay, Peninsula; 8°17'N, 13°11'W; 02 May. 1965.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 40
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Uvariodendron (Engl. & Diels) R.E.Fr., Acta Horti Berg. 10: 51 (1930) = Uvaria L. section Uvariodendron, Engl. & Diels in Engl. Afr. Pfl. VI 8 (1901).
Type species. Uvariodendron fuscum (Benth.) R.E.Fr. (= Uvaria gigantea Engl.).
Description. Shrub to trees 2-30 m tall, D.B.H. 1-35 cm; young branches pubescent to tomentose to glabrous, old branches slightly tomentose to gla- brous. Leaves with margin flat to slightly revolute. Petiole 2.5-35 mm long, 1-9 mm wide, pubescent to tomentose to glabrous. Leaf lamina 65-750 mm long, 20-250 mm wide, length:width ratio 2.1-6.2, elliptic to obovate to oblong, coriaceous, base acute to decurrent to rounded to subcordate, apex acute to acuminate, acumen 0.5-38 mm long; surface above glabrous, sur- face below pubescent to glabrous when young, glabrous when old; midrib impressed above, raised below, glabrous above, pubescent to glabrous below; secondary veins 8-41 pairs, brochidodromous to weakly brochidodromous, impressed above, raised below; tertiary veins reticulate. Inflorescences borne on trunk, on branches or axillary, composed of 1-11 sessile to pedicellate flowers. Flower pedicel 0-65 mm long, 1-9 mm in diameter, pubescent to gla- brous. Flowers bisexual, buds globose to ovoid, sessile to pedicellate, 2-22 mm high, 4-30 mm in diameter, pubescent. Bracts 1 to 6, upper bract 1-35 mm long, 1-50 mm wide, depressed ovate to ovate, generally adpressed, en- closing the bud or semi-clasping the pedicel, pubescent outside, glabrous to pubescent inside. Sepals 3, 3-55 mm long, 2.5-43 mm wide, valvate or im- bricate, free or fused at base, pubescent outside, glabrous inside, green to brown. Outer petals 3, 10-70 mm long, 9-47 mm wide, length:width ratio 0.9-2.5, ovate to elliptic, pubescent outside, puberulent to glabrous inside, cream to brown to wine red outside, cream with dark red at base to wine red inside. Inner petals 3, 10-53 mm long, 5-38 mm wide, length:width ratio 0.9-2.4, elliptic to obovate, pubescent outside, puberulent to glabrous inside, cream to brown to wine red outside, cream with dark red at base to wine red inside. Stamens 200 to 3000, 1-5 mm long, 0.1-0.7 mm wide, anthers linear, connective prolongation truncate. Carpels 5 to 160, 1-7 mm long, 0.5-2.2 mm wide, pubescent, free; stigma 0-2 mm long, 0.5-2 mm wide, coiled, pubescent, generally covered with an exsudate at anthesis. Fruiting pedicel 0-31 mm long, 2-8 mm in diameter, pubescent. Monocarps 1 to 80, 17-90 mm long, 4.5-32 mm wide, length:width ratio 1.3-11, generally cylindrical, pubescent to glabrous, green to orange to red to dark-blue black; sessile to Stipitate; stipe 0-12 mm long, 1-10 mm wide, pubescent to glabrous. Seeds 1-18 per monocarp, uniseriate to biseriate, 3 to 29 mm long, 2-11 mm wide, ellipsoid to semicircular.
Key to Uvariodendron species
1 Largest leaves with lamina < 350 MM IONG................ccesccssssteesesseeesesseeeeens 2 - Largest leaves with lamina > 350 mm IONG...............ccsscccsssseessseeeessseeeeees 13 2 Largest leaves with lamina < 160 MM IONG...............ccessscccesseeeeeeeeeeseeeeees 3 - Largest leaves with lamina > 160 MM IONG...............ccccccessssseesesteeesssteeeeeees 5
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 A
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
3 Plant with strong bergamot scent (bark and crushed leaves), leaves stiff, between coriaceous and cartilaginous, apex acute to shortly acuminate; monocarps cylindrical and tomentose with regular tufts of high hair densi- Tye TeaMZaMigpee re twee coe Me eae re Cee te Ree at Ud. mbagoi
- Plant without bergamot scent, leaves coriaceous, apex attenuate; mono- carps cylindrical and glabrous or ovoid and densely pubescent ............... 4
4 Flower buds ca. 4 mm in diameter, covered by ca. 6 velutinous bracts 5-6 mm long; flowers with ca. 50-75 carpels; monocarps ovoid, densely pubescent, sessile (Kenya) ...........ccccccscccsseeseescsseseeseenseeeees Ud. dzomboense
— Flower buds ca. 6 mm in diameter, covered by 2-5 velutinous bracts ca. 4 mm long; flowers with ca. 5 carpels; monocarps cylindrical, glabrous,
with stipe ca. 12 mm long (Mozambique).................... Ud. mossambicense 5 Sepals fused at base over > 10% of their length ............ cc ceecceesseeesseeeeees 6 - Sepals free or fused at base over < 10% of their length, connivent or imbri- COLO a. «he rers vache ite ag tamer oceans castes ncebiive eae age toute eog'aee dt apiccn noesheuys tee gaataruseiteye gee rae 9
6 Plant with a strong lemon scent; leaves narrowly elliptic, base acute to cuneate, flower sessile with petals 15-25 mm long and 5-15 mm wide (Westand' Gentrali Africae! sce. essccsnetenssnneSetisnecatancass-orelh Ud. angustifolium
- Plants with no lemon scent; leaves elliptic to oblong to obovate, base acute to decurrent; flower pedicellate, or flower sessile with petals 20- SSIMMIMIONG ANG 1 MM ICs ace os ere te te en eee cu eee pee 7
7 Plant with bark reddish peeling off; flower bud globose to ovoid, sessile, > 6 mm high; flower with sepals = 10 mm long and wide (Tanzania)............. Upsetters Peau chitc ee bl aar eee Wetaie, oe ae veettes WS in ee Mec ened Seedy Ud. pycnophyllum
- Plant with bark not reddish and not peeling off; flower bud globose, sub- sessile to pedicellate, < 6 mm high; flower with sepals < 8 mm long........ 8
8 Leaves 170-350 mm long; flowers with sepals 3-5 mm long, outer petals elliptic 15-25 mm long, carpels 20 to 40; fruits with 6 to 11 stipitate (stipe 5-12 mm) monocarps (West Africa) ..........cccccceeeseeeeees Ud. occidentale
- Leaves 159-188 mm long, flowers with sepals 5.5-7 mm long, outer pet- als broadly obovate 11-12 mm long, carpels ca. 7; fruits with 3 to 5 ses-
SileimMONnOGAalpSA KENYA), «nied eee etcetera ce ence Ud. schmidtii 9 Leaves obovate, base decurrent, apex acuminate; flowers with bract ca. 10 mm long, ca. 30 carpels (Gabon)............cccceceseeseeeeees Ud. pilosicarpum
- Leaves elliptic to oblong to obovate, base acute to decurrent or acute to round- ed, apex acute to attenuate; flowers with bract < 6 mm long, < 20 carpels...10 10 Plant with a strong aniseed smell; flowering pedicels 15-65 mm (Kenya, FAMZaague. Wicker eee ed ens) Plate eR Rl Ae er ee Ud. anisatum - Plant with no aniseed smell; flowering pedicels < 28 mm.................:008 11 11. Fresh leaves with strong lemon scent when crushed, leaves = 250 mm (CEN tral ARICA erat wstrste. duweceeiste anise mens raeaoae race pees Ud. citriodorum - Leaves with no lemon scent when crushed, leaves < 220 mm................ 12 12 Leaves 140-220 mm long witha midrib slightly raised above with a central groove all along; flower with imbricate sepals 6-12 mm long, and elliptic petals 16-39 mm long with a slight transversal curvature (Tanzania)........ et Sane AN a BPP ER a een ne AA PBPEy ED RARER. «oe ie AAA) O_AR pede) Ud. kimbozaense - Leaves 70-190 mm long with a midrib slightly impressed above; flower with connivent sepals 3-6.5 mm long, ovate petals 10-20 mm long with a strong transversal curvature (Kenya, Tanzania)..............c:cccse Ud. kirkii
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 42
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
13
14
15
16
“i
18
19
Young branches, petioles, and midrib below the lamina covered with a brown tomentum, generally persisting on older branches (West and Cen- MAIC AD St! Sacchi accent aacciane tunsnteas Ga dash cau decriecearn ee Ud. calophyllum Young branches, petioles, and midrib below the lamina pubescent to gla- brous or covered with long soft hairs quickly falling off................e 14 Leaves with rounded to subcordate base (Tanzania)......Ud. usambarense aves with acute torounded DaSe si) -cd..sr.coeetlevastrocaetel taboo atingoens 15 Monocarps with I:w ratio = 5, very narrowly cylindrical, torulose to torose (i.e. very strongly constricted between the seeds); seeds < 10 mm long
(EASEEATD GC Ghy hee Be deren MP EA cl ALOR ge cst el A ily de Ud. gorgonis Monocarps with I:w ratio < 3.5, cylindrical, not constricted between the SECHS SOAS: o al CATV OIE, ses sateen dee nc eet ania codeag eens 16
Young branches glabrous; flowering pedicel = 10 mm, petals wine red outside and inside; monocarps sparsely pubescent to glabrous (Central PT TOA Vets ecc etsaaseaye cates avin abides ee raat senunltba abreast ce retadresveyrh adhe Ud. connivens Young branches pubescent to glabrous; flower pedicel < 15 mm, petals wine red cream to light yellow outside, cream with dark red steak inside; monocarps pubescent to sparsely PUDESCENT ..............cccecccceeseseceeeeeseeeee 17 Bracts 3-8 mm long and 3-10 mm wide; sepals free, sometimes fused at base, generally imbricate, 5-9 mm long and 5-10 mm wide (Central PUMICE jee cess ee Areas ees ere ee eae ee ee ae Ud. molundense Bracts 8-35 mm long and 10-50 mm wide; sepals fused at base over 20- 50% of their length, 11-55 mm long and 13-43 mm wide.....Ud. fuscum (18) Young branches sparsely pubescent to glabrous; sepals 11-23 mm long and 13-26 mm wide; carpels 20 to 70; fruiting pedicel ca. 5 mm long (Cen- RIANA ACE ye cocae teed ectccna canon sions tesstean gacarra< needa aoe Ud. fuscum var. fuscum Young branches with long soft hairs producing a whitish appearance quickly falling off; sepals 20-55 mm long and 16-43 mm wide; carpels SO: to): 60x truiting pedicel Ociminy LONG sete Reed eed kee 19 Flowering pedicels 0-7.5 mm long, sepals 20-30 mm long and 16-26 mm wide, petals 21-40 mm long and 17-29 mm wide, carpels 50 to 100 (Cen- TADAT ICA onc ators antes cannot colle eet oneal Ud. fuscum var. giganteum Flowering pedicels 10-15 mm long, sepals 30-55 mm long and 30- 43 mm wide, petals 50-70 mm long and 36-47 mm wide, carpels 150 to WG GUA ok, es haw te tale a ns Ud. fuscum var. magnificum
Species descriptions
Uvariodendron angustifolium (Engl. & Diels) R.E.Fr., Acta Horti Berg. 10: 58 (1930) Figs 7E-J, 8
= Uvaria angustifolia Engl. & Diels, Notizbl. K6nigl. Bot. Gart. Berlin 2: 295 (1899);
Uva angustifolia (Engler & Diels) Kuntze, Deutsche Bot. Monatsschr. xxi. 173 (1903). Type. CAMEROON — South-West Region « A. Staudt 742a (holotype: B! (B 10 0153115)), Johann Albrechts-Hohe; 4°10'N, 9°12'E; alt. 400 m; 20 Mar. 1896.
Description. Shrub to tree 3-12 m tall, D.B.H. unknown; young branches sparse- ly pubescent to glabrous, old branches glabrous; plant with strong aromatic
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 43
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
aN
N ANS Ki
‘i R \ NI
\
Figure 7. Uvariodendron connivens (Benth.) R.E.Fr. A leaf B flower, two outer and one inner petal removed C outer petal inner view D stamen, front view. Uvariodendron angustifolium (Engl. & Diels) R.E.Fr. E leaves F flower, semi top view G flower, bottom view showing bracts H flower, bottom view, bracts removed I outer petal, outer view J stamen, front view K carpel, front view and detail of ovules. A-D from Mann 1159 A-K from Vigne 1610. Drawings by Hélene Lamourdedieu, Publications Scientifiques du Muséum national d'Histoire naturelle, Paris.
smell. Leaves with strong lemon smell when crushed. Petiole 3-7.5 mm long, 1-2 mm wide, pubescent to glabrous. Leaf lamina 100-199 mm long, 30- 58 mm wide, length:width ratio 3-4, narrowly elliptic, coriaceous, base acute to cuneate, apex acute to broadly acuminate, acumen 11-14 mm long; surface above glabrous, surface below pubescent to glabrous when young, pubescent at base to glabrous when old; midrib slightly impressed above, raised below, gla-
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 AA
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Latitude
10°N 4
8°N 5
6°N 5
10°W
5 i @ ® ; O O (RNs 9) @ Uvariodendron angustifolium 5oW Oc 5oE 10cE
Longitude
Figure 8. Distribution map of Uvariodendron angustifolium. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
brous above, pubescent to glabrous below; secondary veins 8-14 pairs, weakly brochidodromous, slightly impressed above, raised below; tertiary veins reticu- late. Inflorescences borne on trunk and branches, composed of 1 (sub)sessile flower. Flower pedicel 0-6 mm long, 2-3 mm in diameter, velutinous. Flowers bisexual, buds globose, sessile to shortly pedicellate, 5-8 mm high, 6-8 mm in diameter, sericeous. Bracts 1 to 6, upper bract 6-11 mm long, 9-15 mm wide, ovate, appressed, enclosing the bud, sericeous outside, glabrous inside. Sepals 3,9-13 mm long, 9-13 mm wide, fused at base, slightly imbricate at mid-length, sericeous outside, glabrous inside, color unknown. Outer petals 3, 15-25 mm long, 9-15 mm wide, length:width ratio 1.13-1.78, elliptic to oblong, veluti- nous outside, glabrous inside, yellowish brown outside, crimson with cream margins inside. Inner petals 3, 15-22 mm long, 5-10 mm wide, length:width ratio 1.9-3, obovate, velutinous outside, glabrous inside, yellowish brown out- side, crimson with cream margins inside. Stamens 200 to 300, 3-3.5 mm long, 0.1-0.5 mm wide, anthers linear, connective prolongation truncate. Carpels 7 to 30, 3-4.5 mm long, 1-1.5 mm wide, pubescent, free; stigma 1-2 mm long, 0.8-1.5 mm wide, coiled, pubescent, covered with an exudate at anthesis. Fruit- ing pedicel ca. 5 mm long, 3.5 mm in diameter, pubescent. Monocarps 2 to 10, 23-40 mm long, 17-30 mm wide, length:width ratio ca 1.3, ellipsoid, smooth, sparsely pubescent to glabrous, yellow, with strong lemon smell; shortly stipi- tate, stipe 1-3.5 mm long, 1-2.5 mm wide, pubescent. Seeds 9 to 18 per mono- carp, biseriate, 21 to 28 mm long, ca. 10 mm wide, 2-4 mm thick, semicircular.
Distribution. Endemic to Upper Guinean Domain and Lower Guinean Domain of the Guineo-Congolian Region: Cameroon, Ghana, Ivory Coast, Nigeria. This
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 45
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
species has also been reported in Benin (Bada Amouzoun et al. 2019), but no herbarium specimen was associated with this study. Its presence in Benin can thus not be confirmed.
Habitat and ecology. Lowland mature or secondary rain forests. Altitude: 152-400 ma.s.l.
Phenology. Flowers collected from February to March and November to De- cember. Fruits collected from January to May.
Vernacular names. Ghana: ‘Esuno Kodu’ or ‘Bomborgo Kodu’ in Ashanti (Vigne 1610).
Uses. The fruits are used to flavour the soup (Jones FHI 3480).
Notes. This species can be easily distinguished from the other Uvarioden- dron species by its narrowly elliptic leaves. It also emits a strong citrus scent when fresh, a characteristic shared with other Annonaceae species: Uvarioden- dron citriodorum (Le Thomas) Dagallier & Couvreur and Uvariopsis citrata Cou- vreur & Niangadouma.
Preliminary conservation status. This species is distributed from Cameroon to Ivory Coast. Its EOO is estimated at 186,201 km? and its AOO at 52 km7. It occurs in ca. 10 locations, but the last collection dates back more than 20 years and two thirds of the collections are older than 50 years, suggesting a decline in the number of locations and in AOO. We thus assign a preliminary conservation status of Vulnerable VU under criterion B2ab(ii,iv).
Additional specimens examined. CAMEROON — Central Region * R.W.J. Keay FHI37524 (FHI, K), between Bafia and Likoko; 4°21'N, 9°18'E; 05 Feb. 1958 — South-West Region + D.W. Thomas 6087 (MO, YA); Meme, Vicinity of Lake Barombi, Kumba; 4°39'N, 9°24'E; alt. 300 m; Apr. 1986 * D.W. Thomas 7018 (YA), Cocoa farms along the road between Konye and Bakole; 4°39'N, 9°25'E; alt. 300 m; 25 May. 1987 — Unknown major area « A. Staudt 642 (BM, G, K), Kumba; 4°38'N, 9°25'E; 1896. GHANA — Ashanti Region * C. Vigne 1610 (K, P), Pra River, ashanti; 6°33'54.36'N, 0°57'21.6'E; alt. 152 m; Feb. 1929 —- Western Region ° N.K. Lovi 3964 (K, P), New Tafo E.P; 6°13'N, 0°22'E; 03 Dec. 1954. lvoRY COAST - Bouaflé + C.C.H. Jongkind 4368 (IAGB, MO, WAG), Parc National de la Mar- ahoue; 7°02'N, 6°06'W; alt. 270 m; 13 Feb. 1998 —- Daoukro + A.J.B. Chevalier s.n (P), Morénou: environs du poste de Bangouanou; 6°39'N, 4°12'W; 26 Nov. 1909. NIGERIA — Edo State * B.O. Daramola 94/337 (K, MO), lyekoriomwon, Edo State, about 35 kilometers from Uyo (Ugo ?); 6°05'19.05"N, 6°00'04.46"E; 09 Jan. 1994 — Ondo State * A.P.D. Jones FHI3480 (K); Owo District, Owo forest reserve about 4 miles North of Igbatoro crossing; 5°33'36.36"N, 6°56'06"E; 19 Apr. 1943 + F. Anakwense FHI19702 (K); Akure, Akure Forest Reserve; 7°19'N, 5°02'E; 11 Dec. 1950 — Oyo State « D. Gledhill 817 (K); Ibadan District, Gambari Forest Reserve; 7°08'N, 3°50'E; 02 Feb. 1968.
Uvariodendron anisatum Verdc., Kew Bull. 10(4):596 (1956) Figs 9, 10 Type. KENYA — Nairobi * B. Verdcourt 526 (holotype: EA! (EA000002461); iso-
types: K! (KO00198890, KO00198891), PRE); Nairobi District, in Karura Forest and Thika Gorge; 1°14'S, 36°49'E; 24 Jun. 1951.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 46
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
an CanPeLee cee SOUL EETIOm vLURA OF saTROsL
| jivario op.
© lesfy vrenches. wiy rich green and 1" act opele
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ee
ee =a Figure 9. Uvariodendron anisatum Verdc A entire specimen sheet with young branch and leaves B fruit with four mono- carps (one detached) C stamen, side view D flower and pedicel attached to bark clump, semi-bottom view E detail of flower, bottom view F detail of flower showing sepals, one outer petal removed, semi-top view. A Verdcourt 406 B Verd- court 674 D-F Faden 74/886. Photos Léo-Paul Dagallier.
Description. Shrub to tree 3.5—15 (22) m tall, D.B.H. up to 10 cm; young branches sparsely pubescent to glabrous, old branches glabrous; plant with aniseed smell. Leaves reddish pink when young, dark green when old. Petiole 3-9 mm long, 1.5-4 mm wide, sparsely pubescent to glabrous. Leaf lamina 80-313 mm long, 45-187 mm wide, length:width ratio 2.3-3.1, elliptic to obovate, coriaceous, base acute to decurrent, apex acute to attenuate, sur- face above glabrous, surface below sparsely pubescent to glabrate when young, glabrous when old; midrib impressed above, raised below, glabrous above, sparsely pubescent to glabrous below; secondary veins 12-21 pairs, weakly brochidodromous, impressed above, raised below; tertiary veins re- ticulate. Inflorescences clustered on the trunk or borne on branches, com- posed of 1-3 flowers. Flower pedicel 15-65 mm long, 1-2 mm in diame- ter, pubescent. Flowers bisexual, buds globose, pedicellate, 3.5-6 mm high, 4.5-6 mm in diameter, sericeous. Bracts 1 to 2 at base and 1 towards the upper half of the pedicel, upper bract 2-4.5 mm long, 3-8 mm wide, clasp-
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 47
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Latitude
S5cE 300E 350E A0cE Longitude
Figure 10. Distribution map of Uvariodendron anisatum. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
ing the pedicel, velutinous outside, glabrous inside. Sepals 3, 3.5-6 mm long, 4-8 mm wide, valvate to fused at base over 10 % of their length, velu- tinous outside, glabrous inside, color unknown. Outer petals 3, 10-23 mm long, 9-16 mm wide, length:width ratio 1-1.6, broadly ovate to ovate, velu- tinous outside, glabrous inside, cream outside, cream inside. Inner petals 3, 12.5-15 mm long, 5-9 mm wide, length:width ratio 1.5-2, obovate, shortly velutinous outside, glabrous inside, cream outside, cream inside. Stamens 400 to 500, 1.5-2.5 mm long, 0.1-0.5 mm wide, anthers linear, connective prolongation truncate. Carpels 7 to 12, 2-5 mm long, 1-1.5 mm wide, pubes- cent, free; stigma 1-2 mm long, 1-1.5 mm wide, coiled, pubescent. Fruiting pedicel 21-59 mm long, 2-3 mm in diameter, sparsely pubescent to gla- brous. Monocarps 3 to 14, 38-70 mm long, 13-20 mm wide, length:width ratio 2.3-3.5, cylindrical, longitudinally ridged, slightly constricted between the seeds, slightly acuminate, sparsely pubescent, dark olive green to dark- blue black; sessile to shortly stipitate, stipe O-2 mm long, 3-4.5 mm wide, sparsely pubescent. Seeds 8-18 per monocarp, biseriate, 10 to 12 mm long, 5-8 mm wide, ellipsoid to semicircular.
Distribution. Endemic to Somalia-Masai Region: Kenya and Tanzania.
Habitat and ecology. Submontane rain forests (Sometimes dry forests), of- ten along streams. Altitude: 300-1080 m a.s.I.
Phenology. Flowers collected in January, March, from June to July and from November to December. Fruits collected in January, March, from May to July and from November to December.
Vernacular names. Kenya: ‘Mutongu’ in Meru (Parnell 13340).
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Notes. This species is characterized by a strong aniseed smell (lightly to not noticeable on herbarium specimens), a character unique in the Annonaceae family to my knowledge. Apart from the smell, it closely resembles Uvarioden- dron kirkii and can hardly be differentiated on dry sterile material. In flowers, it can be differentiated from Ud. kirkii by its flower pedicel generally longer (15- 65mm, vs. 5-28 mm), its relatively flat petals with a slight transversal curvature (vs. “boat-shaped” petals, i.e. with a strong transversal curvature). Note that the petals curvature is not easy to rely on dry specimen. In fruits, it can be differen- tiated with a greater fruit pedicel than Ud. kirkii (21-59 mm long, vs. 7-22 mm long). Verdcourt also used the monocarps to differentiate the 2 species, the monocarps of Ud. anisatum being dark blue and with a slight longitudinal ridge, and the monocarps of Ud. kirkii being dull-orange and without any pseudosuture (Verdcourt 1969). However, these 2 characters are no longer valid for a clear differentiation of the 2 species as the specimen Robertson MDE 293, which is Ud. kirkii (no aniseed smell reported, flower pedicel length of ca. 11 mm), has dark blue grey fruits, and several specimens of Ud. kirkii (e.g. Drummond 3983; Gilbert 4967; Greenway 2681) present a slight longitudinal ridge.
Conservation status. This species has been assessed as Vulnerable VU un- der criteria B2ab(ii,iii,iv,v) (Luke et al. 2018).
Additional specimens examined. KENYA - Central + E. Battiscombe 1285 (EA, K); Kiambu District, Kiambu Forest; 1°10'S, 36°49'E; alt. 1700 m; 17 Jun. 1924 + J.L. Moon 811 (K); Kiambu District, Kyambu; 1°11'48.48'S, 36°51'32.76'E; alt. 1737 m; 29 Jul. 1913 — Eastern * H.J. Beentje 4089 (EA); Meru, Kijegge Hill; 0°17'N, 37°57'E; alt. 1400 m; 08 Mar. 1989 + |. Malombe 1368 (EA), Ngaia Forest, Kiegoi village, NE border; 0°14'N, 37°55'E; alt. 1170 m; 22 May. 2008 + L.E. Parnell EA13340 (K); Meru, Lower Imenti Foest Reserve; 0°07'14.88"N, 37°41'52.08"E; 24 Aug. 1965 * M.A. Brunt 1546 (K), Embu Meru road; 0°15'43.26"N, 37°38'23.43"E; 16 Feb. 1964 » R.B. Faden 70/120 (EA, k); Meru District, Lower Imenti Forest, 6 mils. from Meru along Meru — Mikinduri Road; 0°06'N, 37°45'E; alt. 1190 m; 01 Mar. 1970 « S.A.L. Smith 287 (K); Embu District, Kiangombe, northern slopes; 0°33'52.56'N, 37°42'27.72'E; alt. 1550 m; 30 Nov. 2000 » W.R.Q. Luke 7123 (EA); Meru, Ngaia Forest, camp 142; 0°19'N, 38°02'E; alt. 1080 m; 22 Nov. 2000 — K4 Central « H.J. Beentje 1830 (EA, WAG), Nairobi, E. Karura forest near Kiambu R; 1°14'30"S, 36°49'30"E; alt. 1600 m; 13 Jan. 1985 « R.B. Faden 74/886 (K, WAG), Meru District. Lower Imenti Forest, on Meru-Mikinduri Road; 0°04'N, 37°45'E; alt. 1190 m; 26 Jun. 1974 — Nairobi ° B. Verdcourt 3689 (K); Nairobi District, Karura Forest, by Ruaraka R. to W. of main Thika highway; 1°14'S, 36°49'E; 21 Jul. 1963 + B. Verdcourt 406 (B, K, K); Nairobi District, Thika Road House; 1°15'59.57"S, 36°50'04.08"E; alt. 1676 m; 24 Dec. 1950 * B. Verdcourt 674 (K); Nairobi District, Karura Forest; 1°14'S, 36°49'E; 29 Jun. 1952 + E. Polhill 324 (K); Nairobi District, Karura Forest; 1°14'S, 36°49'E; 10 Jan. 1961 + V.G.L. van Someren 95 (G, K); Nairobi District, Karura Forest; 1°14'S, 36°49'E; 13 Mar. 1940. TANZANIA — Kilimanjaro * K.B. Vollesen 96/15 (K), Mkomazi Game Reserve, Ibaya Hill; 3°59'S, 37°47'E; alt. 1350 m; 03 Jun. 1996 » R.A. Abdallah 96/86 (K), Mkomazi National Park, Mkomazi Game Re- serve, Maji Kununua Ridge; 3°53'S, 37°48'E; alt. 1500 m; 07 Jun. 1996 — Pwani -R.P. Sacleux 212 (P), Mandéra (Zanguebar); 6°12'51.22"S, 38°22'37.73"E; Jan. 1889 — Tanga « R.C. Wingfield 2880 (K), Msangasi Forest Reserve, 50 km S of Korogwe; 5°36'55.14'S, 38°27'06.26'E; alt. 300 m; 31 Mar. 1975.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 49
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Uvariodendron calophyllum R.E.Fr., Acta Horti Berg. 10: 63 (1930) Figs:1.1,12
= Uvaria gigantea Engl., Notizbl. K6nigl. Bot. Gart. Berlin 2: 292. (1899) (quoad specimen Zenker 1738).
Type. CAMEROON — South Region « G.A. Zenker 2344 (holotype: B! (B100153116); isotypes: BM! (BM000636669), E!(E00704856), G! (G00412241), GOET! (GOET005732), HBG! (HBG502513), K! (K000198796, K000198797), M! (M0107940), P! (P00362658, P00362659, P00362661), S! (SO7-13393, S07- 13396), WAG! (WAG.1418666)), Bipindi; 3°05'N, 10°25'E; 1901.
Description. Tree 2—20 m tall, D.B.H. 1-32.1 cm; young branches tomentose, old branches slightly tomentose to glabrous. Leaves reddish when young, dark green when old. Petiole 4-25 mm long, 2-9 mm wide, tomentose. Leaf lamina 258-765 mm long, 61-248 mm wide, length:width ratio 2.2-4.9, obovate, cori- aceous, base rounded to slightly truncate, apex acuminate, acumen 6-32 mm long; surface above glabrous, surface below pubescent to glabrous; midrib impressed above, raised below, glabrous above, tomentose below; secondary veins 20-41 pairs, brochidodromous to weakly brochidodromous, impressed above, raised below; tertiary veins reticulate. Inflorescences borne on trunk and branches, composed of 2-3 (sub)sessile flowers. Flower pedicel 0-11 mm long, 4-9 mm in diameter, tomentose. Flowers bisexual, buds globose, sessile, 7-17 mm high, 7-30 mm in diameter, tomentose. Bracts 1 to 6, upper bract 10- 23 mm long, 10-40 mm wide, ovate, appressed, enclosing the bud, tomentose outside, glabrous inside. Sepals 3, 10-27 mm long, 10-26 mm wide, imbricate to fused at base, tomentulose outside, glabrous inside, dark brown outside, reddish inside. Outer petals 3, 15-46 mm long, 10-33 mm wide, length:width ratio 0.9-1.5, broadly elliptic to elliptic, tomentulose outside, glabrous inside, cream outside, cream with dark red at base inside. Inner petals 3, 14-41 mm long, 11-32 mm wide, length:width ratio 1.2—1.9, obovate, shortly tomentulose outside, glabrous inside, cream outside, dark red with cream margins inside. Stamens around 3000, 3.5-4.9 mm long, 0.1-0.5 mm wide, anthers linear, con- nective prolongation truncate. Carpels 35 to ca. 150, 2-5 mm long, 0.5-2 mm wide, pubescent, free; stigma 1-2 mm long, 0.5-2 mm wide, coiled, velutinous, covered with an exudate at anthesis. Fruiting pedicel 1-7 mm long, 4-7 mm in diameter, densely pubescent. Monocarps 3 to 35, 27-55 mm long, 9-25 mm wide, length:width ratio 1.8-3.7, ellipsoid to obovoid, tomentose, brown; sessile to shortly stipitate, stipe 0-10 mm long, 1.5-3 mm wide, tomentose. Seeds 7-13 per monocarp, biseriate, ca. 13 mm long, 8-9 mm wide, semicircular.
Distribution. Element of the Upper Guinean Domain and Lower Guinean Domain of the Guineo-Congolian Region: Cameroon, Gabon, Ghana, lvory Coast, Nigeria.
Habitat and ecology. Lowland mature or old secondary rain forests, near streams. Altitude: 30-140 maz.s.l.
Phenology. Flowers collected from December to May. Fruits collected from March to May, from July to August, and in November.
Vernacular names. Cameroon: ‘Ebom Bulu’ (Parren 223) or ‘Ebom Afame’ (Parren 68) in Bulu/Ewondo.
Notes. This species is close to Uvariodendron connivens and Ud. fuscum var. giganteum by having large obovate leaves (more than 25 cm long). However,
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Figure 11. Uvariodendron calophyllum R.E.Fr. A leaf apex upper side B detail of young branch and leaf base, upper side, note the brown tomentum C detail of young branch and leaf base, lower side D leaf E flower fully open, top view F flower with inner petals still attached to each other, semi-top view G fruit with many monocarps (dried) H flower buds, note the brown tomentum. A, D, H Couvreur 1157 B, C Couvreur 999 E, F Couvreur 1013 G Letouzey 14020. Photos A-F, H Thomas Couvreur, G Léo-Paul Dagallier.
it can easily be distinguished from these three other species as it presents a tomentum of short dense brown matted hairs on the young parts (branches, petioles and lower midrib), producing a brown appearance with whitish reflec- tions. The flower buds and outer petals are also covered outside with a similar brown and dense tomentum. The older parts of the plant are generally glabrous but can also present remnants of the tomentum.
Conservation status. This species is widespread, distributed from Ivory Coast to Gabon. It has been previously assessed as Least Concern LC (Cosi- aux et al. 2019a).
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Latitude
@ Uvariodendron calophyllum
y 300 km
| a )
5oW Oc BoE 10cE 15cE Longitude
Figure 12. Distribution map of Uvariodendron calophyllum. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
Additional specimens examined. CAMEROON -— Central Region * J.N. Asong- anyi 421 (P YA), Ndikiniméki, at Sonossi 26 km W. of Ndikinimeki. Map 1/200 000; 4°45'44.24'N, 10°36'29.26"E; 29 Mar. 1982 — Littoral * A.J.M. Leeuwenberg 5282 (BR, K, MO, P PRE, WAG), 8 km W of Masok; 4°08'N, 10°24'E; alt. 400 m; 31 Mar. 1965 * A.J.M. Leeuwenberg 5282a (K, P WAG), 8 km W. of Masok; 4°08'N, 10°24'E; alt. 400 m; 31 Mar. 1965 + R.G. Letouzey 12352 (P YA), colline entre Tcherikoy et Sokelle Il(30 km NW Eseka) — feuille IGN 1/200 000 EDEA; 3°48'18.03"N, 10°34'32.35"E; 14 Dec. 1973 - North-West Region + E.U. Ujor FHI29281 (FHI, K); Mentchum, Nkom-Wum, Bamenda Prov., Wum Distr., Nkom *- Wum F.R. on German old road leading to Timber Camp by the left; 6°16'N, 10°08'E; 03 Jul. 1951 * R.G. Letouzey 14020 (P WAG, YA), Piste Baji-Tumbo, entre Baji et riviere Chonogbonbon, 55 km NNE Wum; 6°45'N, 10°10'E; 12 Jul. 1975 — South Region « G.A. Zenker 1738 (B (B101178582), BM (BM000636667), COI (COI100004925), E (E00718583), G (G00412236), HBG (HBG502512), K (no barcode), LE (LE00012448), LECB (LECB0000053), M (M0239941), P (P06901474, P06901466, P06901467), WAG (WAG.1418665), WU (WU0025882, WU0025883), Z (Z-000056111, Z-000056112)), Bipindi; 3°05'N, 10°25'E; 1898 = G.A. Zenker s.n (P), Bipinde, Bipindi; 3°05'N, 10°25'E; Apr. 1903 « M.PE. Parren 223 (KRIBI, WAG), About 7 km NE of Ebom. Plot 13, subplot 84, tree 6, coordi- nates: X = 7, Y = 3 m; 3°07'N, 10°45 'E; alt. 500 m; Aug. 1996 » M.PE. Parren 68 (KRIBI, WAG), About 7 km NE of Ebom. Plot 4, subplot 53, tree 9, coordinates: X = 7.5, Y = 8.5m; 3°07'N, 10°45 'E; alt. 500 m; Aug. 1996 « R.G. Letouzey 15272 (P YA), Piste Meyo Ntem-Evouzok, 75 Km W Ambam, entre 1er et 3e bras du Ntem; 2°16'48"N, 10°31'12"E; 28 Nov. 1979 « T.L.P. Couvreur 1157 (K, MPU, P WAG,
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
YA), on road Lolodorf-Bipindi, about half way, near Mbiguiligui village (Mbikili- ki); 3°09'41.51"N, 10°31'52.18'E; alt. 250 m; 26 Feb. 2018 + T.L.R Couvreur 486 (YA), 15 km east from Lélé village; 2°16'17.2"N, 13°17'30.35'E; alt. 578 m; 09 Sep. 2013 —- South-West Region » A. Binuyo FHI35564 (FHI, K, WAG), Kumba Distr. Along the path from Pete to Bopo at the right handside of the road in Southern Bakundu Forest Reserve; 4°31'N, 9°22’E; 23 Feb. 1956 * A.H. Gentry 62407 (MO), Banyong, Batanga area, between Awong and Banyu, ca 15 km W of Manyemen. TRANSECT 2; 5°00'N, 9°10'E; alt. 420 m; 02 May. 1988 * B. Sonké 5610 (MO); Meme, Nguti, Sanctuaire Mbanyang Mbo; 5°21'24"N, 9°32'57’E; alt. 239 m; 14 Apr. 2011 * C.F.A. Onochie FHI30860 (FHI, K), S.Bakundu, S. Bakundu F.R., between Bombe Rest House and Mbalange; 4°27'N, 9°28'E; 19 Mar. 1953 » D.W. Thomas 3322 (K, MO, P, YA), North-eastern corner of Korup National Park; near Baro village; 5°16'N, 9°11'E; alt. 200 m; 24 Mar. 1984 + D.W. Thomas 4549 (MO, YA), Takamanda Forest Reserve; 6°14'N, 9°19'E; alt. 170 m; 21 Mar. 1985 - D.W. Thomas 5965 (K, MO, WAG, YA), 30 km W of Kumba on Mbonge Road; 4°31'N, 9°22’E; alt. 50 m; 26 Mar. 1986 » D.W. Thomas 6090 (P, YA); Meme, from the vicinity of Lake Barombi, Kumba; 4°39'N, 9°24'E; alt. 300 m; Apr. 1986 = D.W. Thomas 7499 (MO, P, WAG, YA); Ndian, Between Baro and Ikenge villag- es, along foot path, in the Korup National Park; 5°15'N, 9°O0'E; alt. 250 m; 01 Apr. 1988 + G.K. Gottsberger 210307/12 (ULM, WAG), c. 20 m from Banyang Mbo Research Station; 5°08'N, 9°30'E; 21 Mar. 2007 « J. Dundas FHI13898 (kK), Southern Bakundu Forest Reserve; 4°30'N, 9°30'E; 19 Feb. 1946 » J. Nemba 64 (K, MO, P WAG, YA, YA), Bolo Forest, 5 kms W of Kumba — Mamfe road near Konye; 4°55'N, 9°36'E; alt. 300 m; 25 Mar. 1986 « J. Olorunfemi FHI30561 (FHI, K), Mungo River F.R., Kumba Distr.: Mumbo — Southern Bakossi; 4°50'N, 9°20'E; 09 May. 1951 * M.R. Cheek 9337 (K, YA), Mungo River F.R., Mungo river forest reserve. c. 1 Km East of bridge, Chained road to S; 4°44'N, 9°33'E; alt. 200 m; 24 Oct. 1998 * R.G. Letouzey 13673 (P, YA), entre Babong et Okurikang, 35 km WSW. Mamfe (feuille IGN 1/200 000 Mamfe); 5°37'02.16'N, 9°02'22.7"E; 29 May. 1994 + T.L.R Couvreur 1013 (MPU, WAG, YA), Bayang Mbo Wildlife Sanc- tuary, after Mbu river; 5°21'19.19"N, 9°30'01.69"E; alt. 242 m; 26 Mar. 2016 = T.L.P. Couvreur 980 (WAG, YA), on top of hill, near Small Ekombe village, 3 km after Kumba on road to Ekondo Titi town; 4°37'22.48"N, 9°22'37.12'E; alt. 615 m; 13 Jan. 2016 « T.L.P. Couvreur 999 (MPU, WAG, YA), Bayang Mbo Wildlife Sanctuary, after Mbu river; 5°21'04.06"N, 9°30'01.78"E; alt. 251 m; 25 Mar. 2016. GABON — Ogooué-Ivindo + J. Florence 1005 (P), Station d'lpassa, 10 km S de Makokou; 0°30'N, 12°45'E; alt. 500 m; 17 Apr. 1978 * N. Hallé 548 (P), Bélinga, mines de fer; 1°08'N, 13°12'E; alt. 700 m; 16 Aug. 1966. GHANA — Ashanti Re- gion + C. Vigne 1611 (K, P), Kwahu Prasu; 6°37'10.2"N, 0°54'27.72'E; Feb. 1929 = H. Abbin GC43343 (K), Tano Ofin Forest Reserve, Tano Ofni F.R; 6°40'N, 2°10'W; 16 Aug. 1972 - Eastern Region « F.R. Irvine 3016 (K), Bunsu; 6°16'21.42'N, 0°27'52.93"E; May. 1938 — Western Region « A.A. Enti FE-2169 (B), Neung For- est Reserve, Takoradi-Tarkwa Road; 5°11'07.08'"N, 1°58'23.52"W; May. 1982 » A.A. Enti FH6705 (K, RP WAG), Enchi Distr., Enchi - Nyankamam; 5°49'N, 2°49'W; May. 1957 + M.C. Merello 1385 (MO), Bia National Park, Bia National Forest and Production Reserve. Secondary logging roads west from MIM Timber Company Camp; 6°24'15'N, 3°02'30"W; alt. 140 m; 04 Mar. 1996. lvorY CoAsT — Adzopé » L. Aké Assi 11501 (G), Forét d'Abongoua; 6°15'N, 3°32'W; 19 Mar. 1971 — Divo + C. Chatelain 679 (G), Forét de I'IRCC de Divo; 5°47'N, 5°17'W; 19 Dec. 1990 « L.
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Aké Assi 8469 (G), Forét de Mopri; 5°46'10.5"N, 4°56'34.87"W; 22 Jan. 1966 - Tiassalé * L. Aké Assi 4290 (G, P), Forét d'Amitioro; 5°52'50.13"N, 4°52'46.45"W; 07 May. 1957. NIGERIA — Cross River State - B.O. Daramola 641 (MO), Ikom Forest Reserve; 5°58'N, 8°42'E; 06 May. 1995 + J.O. Ariwaodo 447 (FHI, WAG); Ikom District, Efraya; 5°53'N, 8°42'E; 25 Mar. 1977 * M.G. Latilo FHI43924 (Kk); lkom District, Cross River North Forest Res., between miles 156 & 157 on Ikom-Namfe road; 5°53'08.13"N, 8°47'51.41"E; 10 May. 1961 + PA. Talbot 123 (K), Oban; 5°13'23.28'N, 8°33'06.9"E; 1911 * PA. Talbot s.n (BM); Calabar, Oban; 5°13'23.28"N, 8°33'06.9"E; 1912 * PPC. van Meer 1490 (WAG), Ekinta River For- est Reserve, Northern part. Near and between pillar 18 and 19; 4°58'N, 8°35'E; 26 Apr. 1971 * PP.C. van Meer 1664 (WAG); Ikom District, Cross River North Forest Reserve. Compt 1 and 2. 15 km SE of Ikom; 5°52'N, 8°46'E; 18 May. 1971 - PPC. van Meer 1736 (WAG); Ikom District, Cross River North Forest Reserve. Compt 1 and 2. 15 km SE of Ikom; 5°52'N, 8°46'E; 20 May. 1971 + R.W.J. Keay FHI28683 (K, P); Ikom District, Cross River North Forest Res.; 5°50'N, 8°50'E; 19 Jan. 1951 — Nassarawa State - A.P.D. Jones FHI16965 (P), Khaya HF nr. Onda enclave; 8°30'N, 7°48'E; 18 Feb. 1946 — Oyo State * C.F.A. Onochie FHI31 539 (k); Ibadan District, c. 14 miles south of Ibadan on the ljebu-Ode road; 7°11'00.66'N, 3°58'13.92"E; 19 Mar. 1958 + D.P. Stanfield FHI44949 (K, MO); Ibadan District, Gambari Forest Reserve; 7°07'59.88'N, 3°49'59.88'E; alt. 80 m; 11 Mar. 1964 = R.W.J. Keay FHI22812 (K); Ibadan District, Ibadan Forest Reserve, c. 22 miles south of Ibadan. School Enumeration area 1948; 7°03'02.43"N, 3°54'20.56"E; 22 Apr. 1948.
Uvariodendron citriodorum (Le Thomas) Dagallier & Couvreur, comb. et stat. nov. urn:lsid:ipni.org:names:77326967-1 Figs 13, 14
=Uvariodendron molundense var. citrata Le Thomas, Fl. Gabon No. 16,283 (1969). Type. GABON — Ogooué-lvindo « N. Hallé 525 (holotype: P! (P00363400), sheet here designated, isotypes: K! (KO00198798, KO00198799), MO! (MO216993, MO216994), P! (P00363398), WAG! (WAG0065739)), Bélinga, mines de fer, sommet de Belvédere; 1°08'N, 13°12'E; alt. 800 m; 15 Aug. 1966.
Description. Tree to shrub 4-5 m tall, D.B.H. unknown; young branches gla- brous, old branches glabrous. Leaves with strong lemon smell when crushed. Petiole 6-10 mm long, 1.5-3.5 mm wide, sparsely pubescent to glabrous. Leaf lamina (183) 250-337 mm long, 72-97 mm wide, length:width ratio 2.3-4.2, elliptic to oblong, coriaceous, base acute to rounded (sometimes minutely de- current at the very base, and decurrent on young leaves), apex attenuate, sur- face above glabrous, surface below glabrous; midrib impressed above, raised below, glabrous above, sparsely pubescent to glabrous below; secondary veins 12-18 pairs, weakly brochidodromous, impressed above, raised below; tertiary veins reticulate. Inflorescences borne on branches or axillary, composed of 1 sessile flower. Flowers bisexual, buds globose, sessile, 5-6 mm high, 5-7 mm in diameter, velutinous. Mature flower unknown, measures taken from flower buds or fruits. Bracts 1 to 4, upper bract ca. 5mm long, ca. 7 mm wide, broadly ovate, semi clasping the pedicel, velutinous outside, glabrous inside. Sepals
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 54
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe — Revision of Uvariodendron and Uvariopsis
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1965
Figure 13. Uvariodendron citriodorum (Le Thomas) Dagallier & Couvreur A entire specimen sheet with branch, leaves and flower buds B flower bud showing bracts, semi-side view C fruit with monocarps, Some monocarps transversally cut, top view D fruit with monocarps, some monocarps transversally cut, side view. A, B Hallé 525 (type) C, D Sosef 2219. Photos Léo-Paul Dagallier.
3, ca. 7 mm long, ca. 6 mm wide (measures taken from bud), imbricate, velu- tinous outside, glabrous inside, color unknown. Outer petals 3, length, shape, indumentum and color unknown. Inner petals 3, length, shape, indumentum and color unknown. Stamens number unknown, ca. 1 mm long, ca. 0.2 mm wide, anthers linear, connective prolongation truncate. Carpels 10 to 20, ca. 2 mm long, ca. 0.4 mm wide, sparsely pubescent, free; stigma 0.5 mm long, 0.5 mm wide, pubescent. Fruiting pedicel 10-12 mm long, 2-5 mm in diameter, pubescent to glabrous. Monocarps 5 to 20, 25-40 mm long, 9-20 mm wide, length:width ratio 1.9-2.9, cylindrical, oblong, straight, truncate or rounded at apex, pubescent to glabrate, pale greyish green to red; sessile to shortly stipi-
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Latitude
2oN 4
004
2084
@ Uvariodendron citriodorum 200 km
100E 150E 20cE Longitude
Figure 14. Distribution map of Uvariodendron citriodorum. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
tate, stipe 0-5 mm long, 3-5 mm wide, pubescent to glabrous. Seeds 9-14 per monocarp, biseriate, 13 to 15 mm long, ca. 11 mm wide, semicircular.
Distribution. Endemic to Lower Guinean Domain of the Guineo-Congolian Region. Known from one area in Gabon: Bélinga, mines de fer, and one locality in Republic of the Congo: Les Saras.
Habitat and ecology. Mature rain forests on rocky soils. Altitude: 800- 950 ma.s.l.
Phenology. Fruits collected in July and November.
Vernacular names. Gabon: ‘Bombamba’ in Bakota (Hallé 2896).
Etymology. The specific epithet refers to the strong lemon smell of the plant. The epithet ‘citrata’ would prevail as it is the one given by Le Thomas for the variety. However, this specific epithet is already taken by Uvariopsis citrata Couvreur & Niangadouma, from the genus Uvariopsis, which is closely related to Uvariodendron. Following the recommendation 23.A.3.h from Turland et al. (2018) (“Avoid [the specific epithets] that have been used before in any closely allied genus”), we choose the specific epithet ‘citriodorum’.
Notes. This species differs from the other species, and particularly from Ud. molundense, in having leaves emitting a strong lemon scent when fresh ma- terial is crushed. Apart from this character, this species is morphologically very similar to Ud. molundense. However, as Ud. citriodorum and Ud. molundense are not monophyletic (Fig. 1, Suppl. materials 1, 2), they can’t be considered the same species following the phylogenetic species concept.
Preliminary conservation status. This species is only known from one lo- cality in Gabon and one locality in the Republic of the Congo. The EOO of
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
the species is estimated at 2,256 km? and its AOO at 20 km?. The unique oc- currence in the Republic of the Congo dates back more than 30 years and the occurrences in Gabon are situated in Bélinga. Although the project of ex- ploitation of the Bélinga iron ore deposits has been canceled, this locality is still threatened by a possible future exploitation of the ore. Following IUCN criterion B, it is thus assigned a preliminary conservation status of Endan- gered EN B1a(i,ii,iii,iv)+2a(i,ii,iii,iv).
Additional specimens examined. GABON — Ogooué-lvindo * M.S.M. Sosef 2219 (BR, K, LBV, MO, WAG), Bélinga, Mines de Fer, 4 km on the road to Mvadi; 1°O5'N, 13°12’'E; alt. 900 m; 05 Nov. 2005 « N. Hallé 2896 (P), Bélinga; 1°05'N, 13°08'E; alt. 900 m; 29 Oct. 1964 + N. Hallé 3082 (P), Bélinga; 1°05'N, 13°08'E; alt. 950 m; 07 Nov. 1964 * N. Hallé 13 (P), Bélinga, mines de fer, route du Bel- védére; 1°05'N, 13°12'E; alt. 950 m; 08 Jul. 1966 « N. Hallé (P), Bélinga, mines de fer, route du pt. B3; 1°06'N, 13°12'E; 25 Jul. 1966 + N. Hallé (K, MO, P), Bélinga, mines de fer; 1°08'N, 13°12’E; alt. 950 m; 16 Jul. 1966. REPUBLIC OF THE CON- Go — Kouilou « H. de Foresta 1759 (P), Les Saras, piste Cofibois, environs de la plantation Coobama de 1987; 4°22'S, 12°22'E; 25 Nov. 1988.
Uvariodendron connivens (Benth.) R.E.Fr., Acta Horti Berg. 10: 55 (1930) Figs 7A-D, 15, 16
=Uvaria connivens Benth., Trans. Linn. Soc. London 23(3): 465 (1862); Uva conniv- ens Kuntze, Revis. Gen. PI. 1: 8. (1891). Type. EQUATORIAL GUINEA — Bioko Sur - G. Mann 1159 (lectotype: K! (KO00198803); isolectotypes: P! (P00362655), K! (KO00198804, KO00198805)), Fernando Po; 3°30'N, 8°40'E; 1861.
= Uvaria winkleri Diels, Bot. Jahrb. Syst. 38(3): 240 (1907). Type. CAMER- OON — South-West Region * H. Winkler 1466 (holotype: B (not found, de- stroyed?)); Moliwe.
= Uvaria megalantha Diels, Bot. Jahrb. Syst. 39(3-4): 472 (1907). Type. CAMER- OON — South Region « G.A. Zenker 3204 (holotype: B (not found, destroyed?); lectotype: WAG! (WAG0057972), designated by Couvreur et al (2022); isolec- totypes: BM! (BM000636652), E! (E00147958), G! (G00412220), GOET! (GOET005733), HBG! (HBG502487), K! (K000198800), L! (L.1768578), M! (M0107939), P! (P01982908), S! (S07-13392), WU! (WU0025787), Z! (Z- 000000876, Z-000000877)), Kamerun. Bipinde; 3°05'N, 10°25'E; 1904.
Description. Tree 3-20 m tall, D.B.H. 2-25 cm; young branches glabrous, old branches glabrous. Petiole 5-21 mm long, 2-6 mm wide, glabrous. Leaf lamina 254-636 mm long, 66-177 mm wide, length:width ratio 2.3-6.2, elliptic to ob- long to obovate, coriaceous, base acute to rounded, sometimes truncate or sub- cordate, apex acute to acuminate, acumen 5-24 mm long; surface above gla- brous, surface below glabrous; midrib impressed above, raised below, glabrous above, glabrous below; secondary veins 16-28 pairs, weakly brochidodromous, impressed above, raised below; tertiary veins reticulate. Inflorescences borne on trunk and branches or axillary, composed of 1 flower. Flower pedicel (5) 10-40 mm long, 1.4-4 mm, increasing toward the apex up to 10 mm in diameter, pu- bescent to glabrous. Flowers bisexual, buds ovoid to globose, pedicellate, 9-22 mm high, 8-30 mm in diameter, pubescent. Bracts 1 to 6, upper bract 4-13 mm
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Figure 15. Uvariodendron connivens (Benth.) R.E.Fr. A young branch with leaves, upper side B detail of petiole and base of leaf, upper side C fruiting material with unripe monocarp, side view D flower, top view E flower, side view F flower bud, top view G flower bud, bottom view H flower, one sepal removed, semi-bottom view. A, B Couvreur 383 C, F, G Couvreur 620 D, E Couvreur 1016 H Couvreur 1051. Photos Thomas Couvreur.
long, 6-17 mm wide, ovate, appressed, enclosing the bud, pubescent outside, glabrous inside. Sepals 3, 5-14 mm long, 7-17 mm wide, imbricate to fused at base, puberulent outside, glabrous inside, dull green. Outer petals 3, 14-32 mm long, 12-29 mm wide, length:width ratio 0.95-1.5, broadly ovate to ovate, pubescent to puberulent outside, puberulent to glabrous inside, wine red (cream in immature flowers) outside, wine red (cream in immature flowers) inside. Inner petals 3, 9.5-30 mm long, 8-23 mm wide, length:width ratio 0.9-1.9, broadly ovate to ovate, pubescent to puberulent outside, puberulent to glabrous inside, wine red (cream in immature flowers) outside, wine red (cream in immature
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Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
10°N 4 AY Ne 8oN5 ap “y v ad bey 6oN 5 ® Oo a = 4oN4 —!
wa a!
— 0 @ Uvariodendron connivens ‘ts a | in aa km BoE 10cE 150E
Longitude
Figure 16. Distribution map of Uvariodendron connivens. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
flowers) inside. Stamens 1900 to 2500, 2-3.8 mm long, 0.3-0.5 mm wide, an- thers linear, connective prolongation truncate. Carpels 5 to 33, 2-6.5 mm long, 0.8-1.5 mm wide, pubescent, free; stigma 0-2 mm long, 1-1.8 mm wide, coiled, pubescent, covered with an exudate at anthesis. Fruiting pedicel 13-31 mm long, 3-8 mm in diameter, glabrous. Monocarps 1 to 10, 22-55 mm long, 17-32 mm wide, length:width ratio 1.3-2, cylindrical to ovoid, longitudinally ridged, sparsely pubescent to glabrous, red to orange when ripe, green when immature; stipe O-8 mm long, 3-10 mm wide, slightly pubescent to glabrous. Seeds 8-23 per monocarp, biseriate, 13 to 29 mm long, 3-14 mm wide, semicircular.
Distribution. Endemic to Lower Guinean Domain of the Guineo-Congolian Region: Cameroon, Equatorial Guinea (Bioko Island) and Nigeria.
Habitat and ecology. Lowland and premontane mature and old secondary rain forests, sometimes in swamp forests. Altitude: 50-1000 m a.sl.
Phenology. Flowers and fruits collected all year.
Vernacular names. Cameroon: ‘Ikeinju’ in Bakweri (Mbani 14).
Uses. The young leaves are eaten (Cheek 5180) and the fruits are used for cough and dye (Mbani 14).
Notes. This species is easily differentiated from the other species by its pet- als being wine red on both sides in mature flowers. Apart from this charac- ter, Ud. connivens resemble Ud. calophyllum and Ud. fuscum in having great leaves (more than 25 cm long). It can be distinguished from these species by being glabrous when young and old, and by having a distinct flower pedicel 10-40 mm long, whereas Ud. calophyllum and Ud. fuscum flowers are subses- sile (flower pedicel 10-15 mm maximum in Ud. fuscum var. magnificum).
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 59
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe — Revision of Uvariodendron and Uvariopsis
Preliminary conservation status. This species has been assessed previous- ly as Near Threatened NT but the assessment needs to be updated (Peguy 1998). Here, the EOO of this species is estimated at 107,423 km? and its AOO at 268 km?. Based solely on AOO value, it would qualify for Endangered, but none of the other B2 sub-criterion are met. It is relatively widespread in Cameroon with more than 10 locations, thus no longer qualifies for Near Threatened NT. Following IUCN criterion B, and it is assigned a preliminary updated conserva- tion status of Least Concern LC.
Additional specimens examined. CAMEROON - Littoral * T.L.P. Couvreur 620 (MPU, YA), Ebo Wildlife Reserve, Djiuma permanent camp. On Djuma-Djuma trail; 4°20'23.59"N, 10°14'41.58'E; alt. 335 m; 14 Feb. 2014 — South Region « G.A. Zen- ker 2624 (B, BM, G, K, L, M, MA, PR. P WAG), Bipindi; 3°05'N, 10°25'E; 1903 « G.A. Zenker 3401 (BM, G, K), Bipinde; 3°05'N, 10°25'E; 1907 « G.A. Zenker 3487 (BM, G, K), Bipinde; 3°05'N, 10°25'E; 1908 * G.A. Zenker 358 (B, G, M, P P U, WAG), Mimfia; 3°04'N, 10°23'E; Sep. 1913 * G.A. Zenker 3845 (BM, kK), Bipindi; 3°05'N, 10°25'E; 1909 + J.J. Bos 5412 (P WAG), 6 km S. of Kribi, 2-4 km E. of Grand Batanga road; 2°53'N, 9°55'E; 26 Sep. 1969 + T.L.P Couvreur 383 (MPU, WAG, YA); Océan, Campo Ma an National Park, 5 km after main entrance; 2°21'19.48'N, 10°15'33.59"E; alt. 300 m; 15 Feb. 2012 + T.L.P. Couvreur 484 (MPU, YA), 15 km east from Lélé village; 2°16'39.39"N, 13°17'37.19"E; alt. 549 m; 09 Sep. 2013 : T.L.P. Couvreur 706 (MPU, WAG, YA), Campo Ma’an National Park, 11 km on trail from Ebinanemeyong village, on road, 7 km from Nyabessan to Campo town; 2°28'25.42'N, 10°20'39.1"E; 14 Feb. 2015 — South-West Region * B.-A. Nkongme- neck 959 (YA); Fako, Idenau, Mt Cameroun, versabt de Idenao. Feuille IGN 1/200 000 Buea/Douala; 4°12'N, 9°05'E; alt. 300 m; 23 Feb. 1985 + C.F. Tekwe 87 (K, SCA, YA), Ilsobi, above Isobe; 4°10'N, 9°00'E; alt. 40 m; 10 Jun. 1992 * D. Kenfack 1507 (MO), Mokoko; 4°27'N, 9°04'00.12"E; 24 Apr. 2001 » D. Kenfack 879 (MO); Ndian, Korup National Park, 11 km from Mundemba, along Fabe road; 5°05'03.43"N, 9°32'20.63"E; alt. 9 m; 11 Jul. 1997 » D.W. Thomas 2264 (K, MO, P WAG, YA); Ndian, Map # NB 32 IV Buea-Douala. South Korup Reserve; 4°55'N, 8°50'E; alt. 50 m; Jul. 1983 * D.W. Thomas 4447 (K, MO, P, YA), forest and mead- ows on the gently sloping side of Mt Cameroun above small Koto village; 4°18'N, 9°06'E; alt. 550 m; 06 Mar. 1985 - D.W. Thomas 5533 (P. YA), forest between Kindonge and small Ekombe, Southern Bakundu Forest Reserve; 4°35'N, 9°23 'E; alt. 200 m; 10 Feb. 1986 « D.W. Thomas 5537 (P YA), at Bonenza, 2 km N of Lim- be-Idenao road; 4°03'N, 9°05'E; alt. 300 m; 10 Feb. 1986 * D.W. Thomas 6928 (P YA), footpath toward Matene from Mbilishe; 6°14'N, 9°26'E; alt. 400 m; 1987 - D.W. Thomas 7961 (MO, P YA), Steep hillside south of Esukutang village; 5°23'N, 9°00'E; alt. 300 m; 25 May. 1988 * D.W. Thomas 9875 (K, SCA, YA), West of the Onge River and ridges on ‘Thump Mount; 4°20'N, 8°57'E; alt. 200 m; 09 Nov. 1993 » F. Nguembock 76 (K); Fako, Mabeta-Moliwe Reserve; 3°58'N, 9°14'E; 10 Mar. 1992 * G. Mann 763 (BM, K), Ambas Bay; 4°01'N, 9°12'E; Feb. 1861 * G.K. Gottsberger 130307/21 (ULM, WAG), c. 300 m from Banyang Mbo Research Sta- tion; 5°08'N, 9°30'E; 13 Mar. 2007 * G.P. Tchouto Mbatchou 685 (K, SCA, YA), Bomana secondary forest. Transect OA, Plot OAQZ; 4°15'N, 9°01'E; alt. 200 m; 05 Oct. 1993 « |. von Rege 87 (K, SCA, YA); Fako, Mabeta, 6 km SE Limbe SBL; 3°59'N, 9°17'E; alt. 60 m; 11 Aug. 1993 * J. Bongyu 73 (K); Fako, Mabeta-Moliwe Reserve; 3°58'N, 9°14'E; 06 Apr. 1992 * J. Nemba 550 (MO, P. YA), Secondary growth and old growth forest along Kumba-Mamfe road at mile 14 Lkiliwindi; 4°44'N, 9°29'E;
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alt. 200 m; 15 Jun. 1987 * J. Nemba 56 (L, PU, YA), 5 kms west of Kumba-Mam- fe road near Konye; 4°55'N, 9°36'E; alt. 300 m; 25 Mar. 1986 * J.-P. Ghogue 1551 (YA), Bimbia Bonadikombo (former Mabeta Moliwe), 18 km SE Limbe; 3°59'36'N, 9°15'43"E; alt. 50 m; 10 Apr. 2003 « J.F. Villiers 2483 (P YA), 4 km E Bomana, 34 NW limbé; 4°12'55.22"N, 9°06'11.21"E; 14 Dec. 1984 + J.I. Wheatley 194 (K, SCA, YA); Fako, Mabeta-Moliwe TC 10; 4°01'N, 9°16'E; alt. 50 m; 20 Apr. 1992 « JI. Wheatley 326 (K, SCA, YA); Fako, Mabeta-Moliwe TD 5835 m; 4°01'N, 9°16'E; alt. 100 m; 24 Jun. 1992 + J.J. Wieringa 45 (WAG); Fako, Limbe, Bakingini, forest above ‘mile 11 village’; 4°04'10"N, 9° 03'50"E; alt. 160 m; 20 Jan. 1994 + J.J. Wie- ringa 5839 (BR, FHO, MO, WAG), Bakingini, at edge of plantation area above Mile 11; 4°04'10.8"N, 9°03'27.6"E; alt. 150 m; 06 Mar. 2007 + J.M. Dalziel 8243 (k), Buea1, Buea to Mayuko; 4°09'N, 9°14'E; 13 Feb. 1927 * J.M. Mbani 14 (K, SCA, YA), Njonji; 4°08'11.04"N, 8°59'22.56"E; alt. 100 m; 13 Feb. 1992 + J.M. Mbani 382 (K, SCA, YA), Ekumbe Mofako, Plot M19; 4°28'N, 9°04'E; 21 May. 1994 + J.P. Watts 245 (K, YA), Moliwe, Makota River watershed.TD 5832 m; 4°00'N, 9°15'E; alt. 100 m; 29 Apr. 1992 * J.P. Watts 394 (K, SCA, YA), c.5 km South East of Moliwe, TF +4000 m; 4°02'N, 9°17'E; alt. 100 m; 09 Jun. 1992 + J.P. Watts 782 (K, SCA, YA), forest to the West of Onge River, about 4 km West of Liwenyi village (c 14 km North of Idenau); 4°23'N, 8°59'E; alt. 260 m; 28 Oct. 1993 » M. Etuge 156 (MA, MO, P, WAG, YA), Bakolle Bakossi, on Kumba — Mamfe road; 5°01'N, 9°40'E; alt. 350 m; 24 May. 1986 « M. Etuge 2390 (K, YA), Max's trail, Nyasoso; 4°49'39.72'N, 9°40'51.96'E; alt. 1100 m; 24 Jun. 1996 > M. Etuge 2396 (K, YA), Max's trail, Nyasoso; 4°49'39.72"N, 9°40'51.96'E; alt. 1100 m; 24 Jun. 1996 + M. Etuge 6506 (YA), Mungo River F.R., Mungo F.R; 4°44'17"N, 9°33'38"E; 22 Feb. 2006 + MLR. Cheek 5180 (K, P SCA, YA), Liwenyi, Low altitude forest on the West bank of the Onge river above the first set of rapids, that is about 1-2 hours walk inland from Enyenge. Grid ref. and alt. approx. Local names and uses from Clement Offu (Enyenge); 4°17'N, 8°58'E; alt. 50 m; 28 Oct. 1993 » M.R. Cheek 5462 (K, SCA, YA), Low altitude forest above oil palm plantation. Reached after c. 40 minutes walk N then E from Njonji. Hunters path to ‘Lake Njonji’. Little farming, but many gaps and fallen trees at low altitude, c. 150-300 m, crossing and running alongside substantial seasonal stream. At c. 400 m, Hypselodelphyus-Aframomum thicket dominates; 4°08'N, 9°01'E; alt. 300 m; 18 Nov. 1993 » M.R. Cheek 8164 (K, YA); Ndian, Korup National Park, Ekundu Kundu, Transect 10, c. 1100 m; 5°08'N, 8°55'E; alt. 170 m; 25 Apr. 1996 * N. Ndam 1076 (K, SCA), Bonjare, Plot 09; 4°26'N, 9°01'E; alt. 220 m; 30 Apr. 1994 * N. Ndam 1118 (K, SCA), Bonjare, Plot 10; 4°26'N, 9°01'E; alt. 270 m; 01 May. 1994 * N. Ndam 708 (K, YA), Bomana-Koto Rd c 500 m Bearing 305deg towards Onge river 3 hr walk from the rd; 4°13'N, 9°04'E; alt. 400 m; 18 Oct. 1993 « P. Nkeng 37 (K, SCA, YA), Etome; 4°03'N, 9°07'E; alt. 300 m; 02 Mar. 1992 - R.G. Letouzey 15175 (P YA); Ndian, Rivieres Mosongosele et de Ndian depuis Mosongosele jusqu’a l'entrée amont de la mangroce, env. 20 km au SW de Mundemba (feuille IGN 1/200 000 Buea-Douala); 4°49'27.3'N, 8°45'15.72'E; 13 Jun. 1976 — R.G. Letouzey 15177 (MO, PP WAG, YA), Au SW de Mosongosele, 20 km WSW Mendumba; 4°54'N, 8°45'E; 14 Jun. 1976 * S. Cable 2329 (K, YA); Ndian, Korup National Park, Ekundu Kundu, path to Esoki about 4 km from Ekundu-Kundu (as on 27"); 5°03'16.8'N, 8°56'58.5'E; alt. 350 m; 29 Apr. 1996 « S. Cable 611 (K, SCA, YA), Dikulu, Coastal lowland rain forest along Man- grove stream; 3°59'N, 9°14'E; alt. 50 m; 17 Dec. 1993 * S.N. Ekema 1078 (K, YA), Mokoko Forest Reserve, Boa/Likinge; 4°24'N, 9°00'E; alt. 150 m; 31 May. 1994 -
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 61
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
T.C.H. Sunderland 1264 (K, SCA, YA), Mabeta-Moliwe: TB 6000 m; 4°03'N, 9°16'E; alt. 40 m; 22 Apr. 1992 * T.C.H. Sunderland 1536 (K, K, SCA, YA), Nyasoso, Mt Kupe: Max's Trail; 4°48'05.04"N, 9°42'29.16"E; alt. 1600 m; 09 Jul. 1992 + T.D. Maitland 537 (K, P), Buea area, at Balifamba; 4°10'N, 9°18'E; alt. 731 m; 1929 « T.L.P. Couvreur 1016 (MPU, WAG, YA), Bayang Mbo Wildlife Sanctuary, after Mbu river; 5°21'26.28'N, 9°30'05.88'E; alt. 253 m; 26 Mar. 2016 + T.L.P. Couvreur 1051 (MPU, WAG, YA), Mt Cameroon National Park, on the Bomona trail, behind Bomo- na village, 10 km NW from Idenau; 4°17'48.27'N, 9°04'43.77'E; alt. 690 m; 03 Apr. 2016 * W.G. Gosline 235 (K, YA), Kupe Village, trail to Kupe rock saddle; 4°47'10'N, 9°41'30"E; alt. 950 m; 28 Nov. 1999 + W.J. Baker 294 (K, SCA, YA); Fako, Mabeta, 6 km SE Limbe SBL; 3°59'N, 9°17'E; 10 Aug. 1993 — Unknown major area + W.G. Gosline 209 (K, WAG, YA), Meme Division, Mahole-Bintulu road; 4°47'30'N, 9°36'12"E; alt. 300 m; 24 Nov. 1999. EQUATORIAL GUINEA — Bioko Norte + M.G. Carvalho 4220 (K, MA), BIOCO: Malabo — Cupapa, km 22-23, margenes del rio Ejoa, 32NMK9005, 200 m; 3°43'12'N, 8°51'36"E; 06 Jul. 1989 — Bioko Sur + W.R.Q. Luke 11955 (EA, K, MA), Moaba — Moka trail, Biadyi River Camp Pt 140; 3°17'06.4'N, 8°38'17.81"E; alt. 650 m; 16 Mar. 2007 * W.R.Q. Luke 13184 (K, MA), Moraka pt 340 to 342; 3°16'13.8'N, 8°28'29.64"E; alt. 3m; 28 Jan. 2009. NIGERIA — Cross River State * C.F.A. Onochie FHI36080X (K); Calabar, Oban Group Forest Reserve, between Akor and Orem; 5°36'N, 8°35'E; 21 Jan. 1957 + E.U. Ujor FHI31636 (K); Calabar, Ikot Ewa; 4°57'24.84"N, 8°38'44.88"E; 05 Jul. 1952 + H.D. Onyeachusim FHI54055 (kK); Calabar, between miles 57-58 Osomba village on Calabar-Mamfe road; 5°27'23.32"N, 8°39'55.34"E; 21 Feb. 1964 +» M.C. Ejiofor FHI21898 (kK); Calabar, Oban Group Forest Reserve; 5°36'N, 8°35'E; 07 May. 1952 - M.G. Latilo 23 (K); Calabar, Akamkpa Rubber Estate. Calabar River Division; 5°18'N, 8°20'E; 21 Mar. 1959 « M.G. Latilo 32 (K, MO); Calabar, Akamkpa Rubber Estate. Dukwe felling area. Calabar River Division; 5°18'N, 8°20'E; 23 Mar. 1959 = PA. Talbot 1254 (BM, K), Oban; 5°13'23.28"N, 8°33'06.9"E; 1911 » PA. Talbot 158 (BM); Calabar, Oban; 5°19'N, 8°34'E; 1911 * PA. Talbot 402 (BM), Oban; 5°13'23.28"N, 8°33'06.9"E; 1911 + PA. Talbot 404 (BM, K), Oban; 5°13'23.28'N, 8°33'06.9"E; 1911 * PA. Talbot 433 (BM), Oban; 5°13'23.28"N, 8°33'06.9"E; 1911 - PA. Talbot 434 (BM), Oban; 5°13'23.28"N, 8°33'06.9"E; 1911 * PA. Talbot 82 (BM, K), Oban; 5°13'23.28"N, 8°33'06.9"E; 1911 » PA. Talbot s.n (BM); Calabar, Oban; 5°13'23.28"N, 8°33'06.9"E; 1912 » PPC. van Meer 1412 (WAG); Calabar, Oban Group Forest Reserve, East Block; 5°31'N, 8°41'E; alt. 200 m; 21 Apr. 1971 - PPC. van Meer 1430 (U); Calabar, Oban Group Forest Reserve, East Block; 5°31'N, 8°41'E; alt. 200 m; 22 Apr. 1971 » PRPC. van Meer 1430 (WAG); Calabar, Oban Group Forest Reserve, East Block; 5°31'N, 8°41'E; alt. 200 m; 22 Apr. 1971 - R.W.J. Keay FHI28191 (K); kom District, Afi River Forest Reserve, near Aboa- bam, forest by river Nkem; 6°11'52.16'N, 8°58'40.48"E; 09 Dec. 1950.
Uvariodendron dzomboense Dagallier, Q.Luke & Couvreur, PhytoKeys 174: 114 (2021) Figs 17, 18; Table 3
Type. KENYA — Coast * S.A. Robertson MDE207 (holotype: K! (no barcode); iso- types: EA!, MO!, WAG! (WAG0065798)), Kwale District - Dzombo Hill; 4°26'S, 39°13'E; alt. 300 m; 07 Feb. 1989.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 62
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Figure 17. Uvariodendron dzomboense Dagallier, Q.Luke & Couvreur A leaf, upper side B petiole and base of leaf, upper side C flower bud showing bracts, side view D flower, two outer petals and three outer petals removed E fruit with young monocarps. A-C Luke 7443 D, E Robertson MDE 207. Photos Léo-Paul Dagallier.
Description. Tree 4—7 m tall, D.B.H. unknown; young branches sparsely pubes- cent to glabrous, old branches glabrous; leaf bud ‘eragrostiform’, composed of 5, distichous, longitudinally folded, velutinous scales. Leaves with margin slightly revolute. Petiole 3-4 mm long, 1-1.5 mm wide, sparsely pubescent to glabrous. Leaf lamina 65-132 mm long, 20-45 mm wide, length:width ratio 2.9-3.6, el- liptic to narrowly elliptic, coriaceous, base acute to slightly decurrent, apex at- tenuate, surface above glabrous, surface below sparsely pubescent to glabrous when young, glabrous when old; midrib impressed above, raised below, glabrous above, slightly pubescent to glabrous below; secondary veins 12-13 pairs, weak- ly brochidodromous, impressed above, raised below; tertiary veins reticulate. In- florescences borne on trunk and branches, composed of 1 flower. Flower pedi- cel 8-30 mm long, 2-2.5 mm in diameter, densely pubescent. Flowers bisexual, buds globose, sessile, ca. 4mm high, ca. 4.5 mm in diameter, sparsely pubescent. Bracts 6 at base of the pedicel in flower bud, generally the uppermost remaining towards the lower half of the pedicel on mature flower, 5-6 mm long, 5-8 mm wide, ovate, pubescent to shortly pubescent outside, glabrous inside. Sepals 3, 5-7 mm long, 4.5-7 mm wide, fused at base, pubescent to shortly pubescent outside, glabrous inside, color unknown. Outer petals 3, ca. 16 mm long, ca. 9 mm wide, length:width ratio ca. 1.8, ovate, shortly velutinous outside, glabrous in- side, color unknown. Inner petals 3, ca. 18 mm long, ca. 8 mm wide, length:width ratio ca. 2.3, obovate, shortly velutinous outside, glabrous inside, color unknown. Stamens 700 to 1000, 2 mm long, 0.5 mm wide, anthers linear, connective pro-
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 63
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Oo
208
Latitude
48
@ Uvariodendron dzomboense — T J £ J T T 200E 25°E 300E 35°E 40cE Longitude
Figure 18. Distribution map of Uvariodendron dzomboense. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
longation truncate. Carpels 50 to 75, ca. 2 mm long, 1-1.5 mm wide, densely pubescent, free; stigma unknown. Fruiting pedicel ca. 14 mm long, ca. 4 mm in diameter, pubescent. Monocarps (unripe?) ca. 35, ca. 15 mm long, ca. 10 mm wide, length:width ratio ca 1.5, ovoid, densely pubescent, golden brown, sessile. Seeds (unripe?) ca. 5 per monocarp, uniseriate, ca. 4.5 mm long, ca. 10 mm wide.
Distribution. Endemic to Somalia-Masai Region. Only known from one local- ity in Kenya: Dzombo Hill.
Habitat and ecology. Moist semi-deciduous forest. Soil: igneous intrusion. Altitude: 270-300 m a.s.I.
Phenology. Flowers collected in January and June. Fruits collected in February.
Notes. This species differs from the other Uvariodendron species by the combination of small (i.e. less than 150 mm long) narrowly elliptic to elliptic leaves and 50-75 densely pubescent carpels. It differs from Ud. kirkii by its smaller leaves (132 mm maximum versus 210 mm maximum) and higher num- ber of carpels (50-75 versus 7-20).
Preliminary conservation status. Previous work estimated the EOO and AOO of this species to be less than 6 km, and assigned a preliminary status of En- dangered EN B1ab(iii)+2ab(iii) (Dagallier et al. 2021).
Additional specimens examined. KENYA — Coast * W.R.Q. Luke 1654 (EA, K); Kwale District, Dzombo Forest Reserve; 4°25'S, 39°13'E; alt. 270 m; 06 Jan. 1989 + W.R.Q. Luke 2884 (EA, K); Kwale District, Dzombo Forest Reserve; 4°25'S, 39°13 E; alt. 271 m; 04 Oct. 1991 + W.R.Q. Luke 3370 (EA); Kwale District, Dzom- bo Forest Reserve; 4°25'S, 39°13'E; alt. 272 m; 12 Nov. 1992 * W.R.Q. Luke 7443 (EA); Kwale District, Dzombo; 4°25'S, 39°12'E; alt. 270 m; 28 Jun. 2001.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 64
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Uvariodendron fuscum (Benth.) R.E.Fr., Acta Horti Berg. 10: 61 (1930) Figs 4, 19-23; Table 4
= Uvaria fusca Benth., Trans. Linn. Soc. London 23(3): 466 (1862); Uva fusca Kuntze, Revis. Gen. Pl. 1: 8 (1891). Type. EQUATORIAL GUINEA — Bioko Sur - G. Mann 308 (holotype: K! (K000198801); isotype: P! (P00362657)); 3°30'N, 8°40'E; alt. 396 m; 1860.
= Uvariodendron mirabile R.E.Fr., Acta Horti Berg. 10 : 59 (1930). Type. CAm- EROON — South-West Region « P.R. Preuss 1378 (lectotype: P! (P00315830), designated by Couvreur et al. (2022), B destroyed), zwischen Victoria und Bimbia; 3°58'58.55'"N, 9°15'19.17°E; 15 Mar. 1898.
= Uvaria gigantea Engl.; Uva gigantea Kuntze; Uvariodendron giganteum (Engl.) R.E.Fr.; concerning Uvariodendron fuscum var. giganteum (see details under this variety).
= Uvariodendron magnificum Verdc.; syn. nov. concerning Uvariodendron fus- cum var. magnificum (see details under this variety).
Description. Tree 3-15 m tall, D.B.H. 5-35 cm; young branches with long soft hairs producing a whitish appearance quickly falling off to glabrous, old branch- es glabrous. Petiole 4-35 mm long, 2-8 mm wide, pilose to glabrous. Leaf lam- ina 160-750 mm long, 43-225 (250) mm wide, length:width ratio (2.1) 2.5-4, narrowly elliptic to elliptic to narrowly obovate, coriaceous, base acute to cu- neate to rounded, apex rounded to acuminate, acumen 1-23 mm long; surface above glabrous, surface below pilose to glabrous when young, glabrous when old; midrib impressed above, raised below, glabrous above, pilose to glabrous below; secondary veins 15-33 pairs, weakly brochidodromous, impressed above, raised below; tertiary veins reticulate. Inflorescences borne on trunk and branches, composed of 1-2 (sub)sessile to pedicellate flowers. Flower ped- icel O-15 mm long, 3-6 mm in diameter, velutinous. Flowers bisexual, buds globose, sessile, 6-15 mm high, 6.5-15 mm in diameter, velutinous. Bracts 1 to 6, upper bract 8-35 mm long, 10-50 mm wide, broadly ovate, clasping the pedicel, enclosing the sepals, pubescent outside, glabrous inside. Sepals 3, 11-55 mm long, 13-43 mm wide, ovate, fused at base over 20-50% of their length, velutinous outside, glabrous inside, brown. Outer petals 3, 20-70 mm long, 17-47 mm wide, length:width ratio 1.1—-1.7, elliptic to broadly ovate, veluti- nous outside, glabrous inside, cream to greenish outside, cream with a dark red streak from base up to 75% of the petal length inside. Inner petals 3, 20-53 mm long, 15-38 mm wide, length:width ratio 1.1-2.1, elliptic to broadly obovate to obovate, puberulent outside, glabrous inside, cream outside, dark red to dark purplish red with cream margins inside. Stamens around 2500, 3.5-5 mm long, 0.1-0.5 mm wide, anthers linear, connective prolongation truncate, pale yellow. Carpels 20 to 160, 4-7 mm long, 0.5-2.2 mm wide, velutinous, free; stigma 1-2 mm long, 0.8-1.1 mm wide, coiled, glabrous to velutinous, covered with an exudate at anthesis. Fruiting pedicel 5-18 mm long, 5-8 mm in diameter, pubescent. Monocarps 6 to 80, 20-60 mm long, 11-32 mm wide, length:width ratio 1.7—2.5, cylindrical, curved, acuminate, puberulent, green to brown; sessile to shortly stipitate, stipe O-4 mm long, 2-5 mm wide, pubescent to glabrate. Seeds 1-16 per monocarp, biseriate, 14 to 23 mm long, 7-11 mm wide, semi- circular, orange-brown.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 65
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Distribution. Element of the Lower Guinean Domain and Congolia Domain of the Guineo-Congolian Region and Zambezian Region: Cameroon, Democratic Republic of the Congo, Gabon, Equatorial Guinea (Bioko Island), Nigeria, Uganda.
Habitat and ecology. Lowland and submontane to mountain mature or old secondary rain forests. Altitude: 100-1400 m a.s.I.
Phenology. Flowers collected from January to April. Fruits collected from March to April.
Vernacular names. Cameroon: ‘Limboto’ in Bakweri (van Andel 3761), ‘Obom Ossoé’ in Yaoundé (Biholong 279). Gabon: ‘Inkaca’ in Bakota (Hallé 3156).
Uses. The young leaves are boiled and used for soup (Cheek 5145) and the ripe fruits are eaten (van Andel 3761).
Notes. From now on, the name Ud. fuscum encompasses the synonyms Ud. mirabile, Ud. giganteum and Ud. magnificum. Ud. fuscum consists of a large morphological variation of the leaf and flower size, with var. magnificum having the largest dimensions, followed by var. giganteum and then the type variety being the smallest (Fig. 4, Table 4). Although this variation seems to form a continuum, we recognize three different morphological groups described as va- rieties (see notes under the varieties). This species resembles Ud. calophyllum, Ud. connivens and Ud. usambarense in having large elliptic to obovate leaves. It differs from Ud. calophyllum and Ud. connivens in having pilose to glabrous young branches and petioles (vs. tomentose in Ud. calophyllum and completely glabrous in Ud. connivens). It differs from Ud. connivens in having flower pedi- cels between 0 and 15 mm long (vs. between 10 and 40 mm long) and in having cream petals with dark red streak within the flower (vs. wine red petals both inside and outside).
Preliminary conservation status. This species is widespread, distributed from Nigeria to Uganda. A previous assessment listed it as Near Threatened NT (Cheek and Cable 2000). However, the assessment was made on what is now Ud. fuscum var. fuscum and thus needs to be updated. Here, the EOO is estimated at 755,899 km? and its AOO at 152 km2. Based solely on AOO value, it would qualify for Endangered EN, but none of the other B2 subcriterion are met. Following IUCN criterion B, it is assigned a preliminary conservation updated status of Least Concern LC.
Uvariodendron fuscum var. fuscum Figs 19, 23; Table 4
Description. Young branches sparsely pubescent to glabrous. Petiole 4-16 mm long, 2-5 mm wide. Leaf lamina 160-450 mm long, 43-118 mm wide, length:width ratio (2.1) 2.8-3.9, Base acute, apex acute to acuminate, sur- face below glabrate when young, glabrous when old; midrib sparsely pubescent to glabrous below; secondary veins 15-24 pairs. Flower pedicel 0-5 mm long. Bracts 1 to 6, upper bract 10-25 mm long, 14-25 mm wide. Sepals 11-23 mm long, 13-26 mm wide. Outer petals 20-39 mm long, 17-26 mm wide. Inner pet- als 20-42 mm long, 15-26 mm wide, length:width ratio 1.3-2.1, broadly obo- vate to obovate. Carpels 20 to 70. Fruiting pedicel ca. 5 mm long. Monocarps (only unripe fruits seen).
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 66
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
: Ns Ciba hg
Figure 19. Uvariodendron fuscum (Benth.) R.E.Fr. var. fuscum A leaf, lower side B apex of young branch with detail of peti- ole and leaf base, upper side, inset: detail of sparse pubescence on young branch C trunk with flower bud (top) and flower (bottom) D open flower E young fruit with unripe monocarps, one old petal remaining F flower semi-bottom view, show- ing bracts and sepals G detail of flower after anthesis, note the falling stamens and pollinator insects, inset: detail of
Coleoptera full of pollen grains. A, E, G Couvreur 1046 B, C Couvreur 1029 D, F Couvreur 990. Photos Thomas Couvreur.
Distribution. Endemic to Lower Guinean Domain of the Guineo-Congolian Region: Cameroon, Equatorial Guinea (Bioko Island), Nigeria.
Habitat and ecology. Submontane to mountain mature or old secondary rain forests. Altitude: 800-1400 maz.s.l.
Additional specimens examined. CAMEROON — South-West Region = A. Dahl 622 (kK), trail north of Likombe village; 4°14'N, 9°11'E; alt. 1060 m; 02 Mar. 1995 + B.-A. Nkongmeneck 891 (YA), Mt Cameroun, flanc d'Ekona Lelu, feuille IGN: 1/200 000 Buea-Douala; 4°16'N, 9°18'E; alt. 1300 m; 14 Jan. 1985 + D.W.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 67
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Thomas 4469 (K, MO, P, P, YA), forest and meadows on the gently sloping side of Mt Cameroun above small Koto village; 4°18'N, 9°06'E; alt. 550 m; 06 Mar. 1985 - E.W.G. Kalbreyer 41 (K); 4°01'N, 9°12'E; 1877 * G.W.J. Mildbraed 10720 (K), Likomba — Pflangzung, 15-35 km NE of Victoria; 4°06'N, 9°20'E; alt. 50 m; Nov. 1928 » H. Lehmbach 178 (B), Buea; 4°09'N, 9°14'E; alt. 1800 m; 16 Jan. 1898 * H. Lehmbach 57 (B, K), Buea1, Buea; 4°09'N, 9°14'E; alt. 1000 m; 26 Apr. 1897 « J.J. Wieringa 2058 (WAG); Fako, Mt Etinde (=Small Mt Cameroon), near and at summit; 4°05'N, 9°07'E; alt. 1400 m; 29 Jan. 1994 - M. Groves 122 (K, SCA, YA), trail north of Likombe Village; 4°14'N, 9°11'E; alt. 1000 m; 21 Feb. 1995 * M.R. Cheek 5145 (K, SCA, YA), Liwenyi, on the West bank of the Onge river above the first set of rapids, that is about 1-2 hours walk inland from Enyenge; 4°17'N, 8°58'E; alt. 50 m; 27 Oct. 1993 » P Lane 142 (K, SCA, YA), Mt Kupé, within Permanent Sample Plot on Shrike Trail leading from Nyasoso to summit; 4°50'N, 9°40'E; alt. 1200 m; 20 Jun. 1994 * R.W.J. Keay FHI37485 (FHI, K), Kumba Distr., eastern boundary of Bambuko F.R., about 11 miles SSW. of Musome. Northern slopes of Cameroon Mt; 4°18'18.11'N, 9°11'55.75'E; alt. 1000 m; 01 Feb. 1958 « S. Cable 1353 (K, SCA, YA), path towards grassland and top of Mt Cameroon from Likombe; 4°07'N, 9°11'E; alt. 1060 m; 22 Feb. 1995 - S. Cable 1524 (K, SCA, YA), Upper Boando, logging path that becomes trail to summit; 4°04'N, 9°09'E; alt. 900 m; 14 Mar. 1995+ S. Cable 1626 (K, YA), path to summit of Etinde from Upper Boando; 4°04'N, 9°09'E; alt. 1000 m; 16 Mar. 1995 + S. Cable 2187 (K, YA); Ndian, Korup National Park, Ekundu Kundu, path from Ekundu-Kundu to about 1 km; 5°02'14.24'N, 8°54'58.14'E; alt. 300 m; 26 Apr. 1996 « T.D. Maitland 453 (K), Buea, above upper farm; 4°09'N, 9°14'E; alt. 1219 m; 1924 + T.D. Maitland s.n.10 (K), Cameroon mountain, Buea; 4°09'N, 9°14'E; alt. 975 m; 1930 + T.D. Maitland s.n.9 (K), Cameroon mountain, Buea area; 4°09'N, 9°14'E; alt. 1219 m; 1930 + T.L.B Couvreur 1026 (WAG, YA), on trail leading to top of Mt Etinde, after Ekonjo village; 4°04'02.27'N, 9°09'10.16'E; alt. 749 m; 01 Apr. 2016 « T.L.P. Couvreur 1029 (MPU, WAG, YA), on trail leading to top of Mt Etinde, after Ekonjo village; 4°04'04.83'N, 9°09'11.43'E; alt. 781 m; 01 Apr. 2016 + T.L.P. Couvreur 1040 (MPU, WAG, YA), Mt Cameroon National Park, Bakinguili trail, above Bakinguili village; 4°05'48.05'N, 9°03'24.71'E; alt. 563 m; 02 Apr. 2016 « T.L.P. Couvreur 1046 (MPU, WAG, YA), Mt Cameroon National Park, on the Bomona trail, behind Bomona village, 10 km NW from Idenau; 4°17'46.46'N, 9°06'06.31'E; alt. 859 m; 03 Apr. 2016 + T.L.P. Couvreur 990 (MPU, WAG, YA), slopes of Mt Cameroon, on the Bokwango trail, near Bok- wango village, 4 km south west of Buea; 4°07'25.26'N, 9°11'11.28'E; alt. 1227 m; 23 Mar. 2016 « T.L.P. Couvreur 992 (MPU, WAG, YA), slopes of Mt Camer- oon, on the Bokwango trail, near Bokwango village, 4 km south west of Buea; 4°07'27.06'N, 9°10'13.93'E; alt. 1560 m; 23 Mar. 2016. EQUATORIAL GUINEA — Bioco (Fernando Poo) « G.W.J. Mildbraed 6428 (B), Pico Basilé, Fernando Poo: Nordseite d. Pics v. Sta. Isabel oberhalb Basile, Wald Uber der Kakao-Region 6-800 m, viel Allanblackia, (oberer Tropenwald); 3°41'24.72'N, 8°51'27.72'E; alt. 800 m; 16 Aug. 1911 — Bioko Sur * W.R.Q. Luke 12203 (MA), Moeri: Camp1 to Camp2; 3°28'09.84'N, 8°40'06.96'E; alt. 704 m + W.R.Q. Luke 13279 (K), Hor- miga Camp pt 346 to North camp pt 347; 3°20'51'N, 8°29'23.64'E; alt. 800 m; 01 Feb. 2009. NIGERIA — Cross River State » K. Schmitt 323 (MO), Cross River National Park. Oban Hills. SW facing slope ca 5 km E of Neghe; 5°15'20"N, 8°38'50"E; 07 Feb. 1995.
PhytoKeys 233: 1-200 (2023), DOI: 10.3897/phytokeys.233.103096 68
Léo-Paul M. J. Dagallier et al.: Systematics of the Monodoreae tribe - Revision of Uvariodendron and Uvariopsis
Uvariodendron fuscum var. giganteum (R.E.Fr.) Dagallier & Couvreur, PhytoKeys 207: 423 (2022) Figs 20, 21, 23; Table 4
= Uvaria gigantea Engl., Notizbl. Konigl. Bot. Gart. Berlin 2: 292. 1899 (quoad specimens Zenker 108 and 698); Uva gigantea Kuntze, Deutsche Bot. Mon- atsschr. xxi. 173 (1903); Uvariodendron giganteum (Engl.) R.E.Fr., Acta Horti Berg. 10: 62 (1930). Type. CAMEROON — Central Region : G.A. Zenker 108 (lectotype: P! (P00362654), designated by Couvreur et al. (2022); isolecto- type: COI! (CO100004926); lectotype designed by Fries (1930) as B, but sheet destroyed), Yaoundé, Yaunde; 3°52'N, 11°31'E; alt. 800 m; 1895.
Description. Young branches with long soft hairs producing a whitish ap- pearance quickly falling off. Petiole 8-35 mm long, 3.5-8 mm wide. Leaf lamina 357-676 mm long, 84-225 mm wide, length:width ratio 2.5-4, base acute to rounded, apex acute to acuminate, surface below pilose to glabrous when young, glabrous when old; midrib pilose to glabrous below; secondary veins 22-33 pairs. Flower pedicel 0O-7.5 mm long. Bracts 1 to 6, upper bract 16-22 mm long, 20-50 mm wide. Sepals 20-30 mm long, 16-26 mm wide. Outer petals 25-40 mm long, 17-30 mm wide. Inner petals 21-40 mm long, 17-29 mm wide, length:width ratio 1.1-1.5, broadly obovate to obovate. Car- pels 50 to 100. Fruiting pedicel 9-15 mm long. Monocarps 6 to 24, 20-50 mm long, 11-25 mm wide, length:width ratio 1.7-3.8, cylindrical, curved, acumi- nate, slightly constricted between the seeds, puberulent, green to brown. Seeds 8-14 per monocarp, ca. 14 mm long, ca. 7 mm wide.
Distribution. Element of the Lower Guinean Domain and Congolia Domain of the Guineo-Congolian Region: Cameroon, Democratic Republic of the Congo, Gabon.
Habitat and ecology. Lowland to submontane mature or old secondary rain forests, on inundated soils or along streams or rivers. Altitude: 100-1300 maz.s.I.
Notes. Ud. fuscum var. giganteum differs from the type variety in having young branches and petiole covered with long soft hairs producing a whitish appearance quickly falling off (vs. young branches and petiole sparsely pu- bescent to glabrous). Compared to the type variety, it has larger leaves (35.7- 67.6 cm long and 8.4—22.5 cm wide, vs. 16-45 cm long and 4.3-11.8 cm wide), with generally more secondary veins (22 to 33 vs. 15 to 24), and flowers with generally greater sepals (20-30 mm long vs. 11-23 mm long) and more car- pels (50 to 100 vs. 20 to 70) (Fig. 4, Table 4). Most of these characters overlap and without the young branches covered with long soft hairs it can be hard to place some specimens in the var. giganteum with certainty. The specimen Zenker 108, defined to be the type specimen by Fries (1930), was not found in B (lost or destroyed), so we made the duplicate from P as the lectotype and the duplicate from COI as the isolectotype (Couvreur et al 2022).
Additional specimens examined. CAMEROON - Central Region * G.A. Zenker 698 (B), Yaoundé, Yaunde; 3°52'N, 11°31'E; alt. 800 m; 04 Feb. 1895 + T.L.P. Cou- vreur 419 (MPU, WAG, YA), Mont Mbam Minkon, on trail, 5 km from Nkol Nyada village; 3°58'04.91'N, 11°24'08.64'E; alt. 1000 m; 21 Mar. 2013 —- East Region ° T.L.P. Couvreur 1206 (MPU, WAG, YA), 60 km south of Yokadouma, 30 km after Ngato, 15 km after river. ALPICAM ‘base de vie’, then on forestry road start- ing 4 km before Maséa village; 3°09'55.18'N, 14°42'25.64'E; alt. 587 m; 05 Mar.
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Figure 20. Uvariodendron fuscum var. giganteum (R.E.Fr.) Dagallier & Couvreur A young branch with leaves, lower side, inset: detail of midrib, note the long soft hairs producing A whitish appearance B young branch, petiole and base of leaf, upper side, note the absence of hairs (fallen off) C flower, top view D flower, side view showing sepals and bracts E young fruit, top view. A Couvreur 1229 B-D Couvreur 1057. Photos Thomas Couvreur.
2019 « T.L.P. Couvreur 1229 (MPU, WAG, YA), 60 km south of Yokadouma, 30 km after Ngato, 15 km after river. ALPICAM ‘base de vie’, then 40 km on forestry road starting 4 km before Maséa village. Coupe 4—4 of UFA 023; 3°05'08.17'N, 14°40'18.2'E; alt. 622 m; 08 Mar. 2019 — South Region « G.A. Zenker 1438 (L), Bipinde, Urwaldgebiet; 3°05'N, 10°25'E; 1898 + M. Biholong 279 (P, YA), prés d‘Alati. Ancienne piste Alati - Mintom Il; 2°11'44.45'N, 13°24'17.61'E; 17 Jan. 1975 — South-West Region » C. Doumenge 473 (L, MO, P), Cameroon. Bakossi Mountains 1-8 Km NNE of Menyum Village; 5°01'N, 9°38'E; alt. 1000 m; 22 May. 1987 » P Lane 501 (K, SCA, WAG, YA), Mt Kupe Division. Ndum. Forest trail 2 km south from Etube-Tape village; 4°51'N, 9°42'E; alt. 1200 m; 02 Feb. 1995 - T.L.P. Couvreur 1057 (MPU, WAG, YA), Nyasoso village, on max's trail to Mt Kupe; 4°49'27.88'N, 9°41'59.42'E; alt. 1227 m; 05 Apr. 2016 « T.L.P. Couvreur 512 (MPU, YA); Fako, on trail from Ekongo village, located 5 km before the entrance to Limbe, 7 km on secondary road. On flank of Mt Etinde. 100 m in Mont Cam- eroon National Park; 4°04'19.23'N, 9°08'00.76'E; alt. 959 m; 16 Oct. 2013 ° T.R. van Andel 3761 (MO, SCA, U, WAG), Bokwango. Trail to Mann's spring; 4°07'44'N, 9°11'26'E; alt. 1130 m; 21 Jun. 2001. DEMOCRATIC REPUBLIC OF THE CONGO -— Ori- entale * T.B. Hart 910 (WAG); Mambasa, Epulu, Zaire, Zone de Mambasa (Ituri); 1°25'N, 28°35 'E; alt. 750 m; 23 Mar. 1989. GABON — Estuaire ° T.-J. Klaine 1690 (P), Environs de Libreville; 0°25'N, 9°27'E; 18 Oct. 1899 — Ogooué-Ivindo * N.
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Figure 21. Uvariodendron fuscum var. giganteum (R.E.Fr.) Dagallier & Couvreur A leaf B flower bud, side view C flower bud, bracts removed, side view D detail of flower bud, two sepals, one outer and two inner petals removed E outer petal, outer view F inner petal, outer view G stamen H carpels, side view and detail of ovules I longitudinal section of receptacle J floral diagram K fruit, longitudinal sections of monocarps. A-K from Hallé 3156 (as Ud. giganteum). Drawings by Héléne Lamourdedieu, modified from Le Thomas (1969; pl. 50, p. 279), Publications Scientifiques du Muséum national d’Histoire naturelle, Paris.
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Hallé 3156 (P), Bélinga; 1°05'N, 13°08'E; 12 Nov. 1964 « N. Hallé 430 (K, P), Bél- inga, mines de fer, le long de la riviére Folley; 1°07'N, 13°11'E; 12 Aug. 1966 * N. Hallé 549 (K, P), Bélinga, mines de fer; 1°08'N, 13°12'E; alt. 700 m; 16 Aug. 1966.
Uvariodendron fuscum var. magnificum (Verdc.) Dagallier & Couvreur, comb. et stat. nov.
urn:lsid:ipni.org:names:77326968-1
Figs 22, 23
= Uvariodendron magnificum Verdc. syn. nov., Kew Bull. 23(3): 515 (1969). Type. UGANDA — Western Province * Okodi in Hamilton 696 (holotype: K! (K000198899, KO00198900, K000198896, KO00198897, KO00198898); iso- types: ENT, MHU! (MHU000022, MHU000023, MHU000024)); Ankole District, Kashoya * Kitomi CFR; 0°13'N, 30°15'E; alt. 1050 m; 15 Jun. 1968.
Description. Young branches with long soft hairs producing a whitish appearance quickly falling off. Petiole 6-20 mm long, ca. 5 mm wide. Leaf lamina 210-750 mm long, 57-215 (250) mm wide, length:width ratio 3-4, base acute to cuneate, apex rounded to acuminate, surface below pilose to glabrous when young, gla- brous when old; midrib pilose to glabrous below; secondary veins 23-30 pairs. Flower pedicel 10-15 mm long. Flower not seen, description from Verdcourt (1969). Bracts 5 to 6, upper bract 8-35 mm long, 10-40 mm wide. Sepals 30-55 mm long, 30-43 mm wide. Outer petals 60-70 mm long, 43-47 mm wide. Inner petals 50-53 mm long, 36-38 mm wide, length:width ratio ca. 1.4, elliptic, imbri- cate at apex. Carpels 150 to 160. Fruiting pedicel 13-18 mm long. Monocarps 10 to 80, 28-60 mm long, 13-32 mm wide, length:width ratio 1.9-2.5, cylindrical, curved, acuminate, pubescent, brownish, fruits not seen, data from Verdcourt (1969). Seeds 1-16 per monocarp, 18 to 23 mm long, 10-11 mm wide.
Distribution. Endemic to Zambezian Region. Known from only one locality in the Western Province in Uganda.
Habitat and ecology. Montane forest. Altitude: around 1050 maz.s.l.
Notes. Ud. fuscum var. magnificum differs from the type variety in hav- ing young branches and petioles covered with long soft white hairs produc- ing a whitish appearance quickly falling off (vs. young branches and petiole sparsely pubescent to glabrous). Compared to the type variety, it has larger leaves (21.-75 cm long and 5.7—21.5 (25) cm wide, vs. 16-45 cm long and 4.3-11.8 cm wide), with more secondary veins (23 to 30 vs. 15 to 24). It differs from the type variety and from the var. giganteum by its flowers having longer pedicels 10-15 mm long (vs. 0-7.5 mm long), larger sepals (30-55 mm long and 30-43 mm wide, vs. 11-30 mm long and 13-26 mm wide), larger petals (50-70 mm long and 36-47 mm wide, vs. 20-40 mm long and 15-30 mm wide) and more carpels (150 to 160 vs. 20 to 100) (Fig. 4, Table 4). This variety is known from two specimens collected more than 50 years ago in the Kasyo- ha-Kitomi Forest Reserve. Uganda's forests have been reported to be degraded (Obua et al. 2010) so this variety might be threatened.
Additional specimens examined. UGANDA — Western Province « T. Syn- nott 197 (MHU); Ankole District, North border of Kitomi Forest; 0°07'29.07'N, 30°18'07.11'E; alt. 1070 m; 22 Oct. 1968.
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Figure 22. Uvariodendron fuscum var. magnificum (Verdc.) Dagallier & Couvreur A young branch with leaves and apical bud B leaf, upper side C longitudinal section of flower bud D flower, semi-side view E carpel with carpel wall partially removed to show arrangement of ovules, side view F young fruit, side view G monocarp, side view H seed, side view. A-H from Okodi in Hamilton 696 (as Ud. magnificum). Drawings by Mary Griesrson, modified from Verdcourt (1969;
fig. 2, p. 517), Kew Bulletin 1969, © Board of Trustees of the Royal Botanic Gardens, Kew.
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Latitude
Oo
@ Uvariodendron fuscum var. fuscum @ Uvariodendron fuscum var. giganteum
@ Uvariodendron fuscum var. magnificum 100E 20°E Longitude
Figure 23. Distribution map of Uvariodendron fuscum. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
Uvariodendron gorgonis Verdc., Kew Bull. 23(3): 512 (1969) Figs 24-26
Type. KENYA — Coast * B. Verdcourt 3940 (holotype: K! (K000198893), sheet here designated; isotype: BR! (BRO000008824325), EA! (EA000002458, EA000002460, EA000002459), K! (KO00198894, K000198892, K000198895); Kwale District, Mrima hill (about halfway up road to Lungalunga from Mwamb- weni); 4°29'06.81'S, 39°15'47.19'E; alt. 182 m; 16 Jan. 1964.
Description. Tree 3-27 m tall, D.B.H. 3-50 cm; young branches pubescent to glabrous, old branches glabrous; plant with lemon smell. Leaf bud ‘eragrosti- form’, composed of 6-12, distichous, longitudinally folded, velutinous scales. Petiole 4-18 mm long, 1.5-—5 mm wide, sparsely pubescent to glabrous. Leaf lamina 153-410 mm long, 36-127 mm wide, length:width ratio 2.3-4.3, elliptic to oblong to obovate, coriaceous, base generally acute to rounded, and minutely decurrent at the extreme base, apex generally acute to acuminate but can also appear rounded or retuse, acumen 0.5-12 mm long; surface above glabrous, surface below sparsely pubescent to glabrous when young, glabrous when old; midrib impressed above, raised below, glabrous above, sparsely pubescent to glabrous below; secondary veins 13-22 pairs, weakly brochidodromous, im- pressed above, raised below; tertiary veins reticulate. Inflorescences borne on trunk and branches, composed of 1-3 flowers. Flower pedicel 8-18 mm long, 3-8 mm in diameter, velutinous. Flowers bisexual, buds globose, sessile, 7-15 mm high, 9-14 mm in diameter, velutinous. Bracts 1 to 8, upper bract 3-12 mm long, 9-25 mm wide, broadly ovate, clasping the pedicel, enclosing
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Figure 24. Uvariodendron gorgonis Verdc A habit B trunk and branches, note the young fruits all along the branches and trunk C young branches and leaves, upper side D young fruit, side view E flower, bottom view F flower, side view, inset: Coleoptera larvae frequently found in the flower. A, B no specimen associated C Dagallier 52 D, E Dagallier 38. Photos Léo-Paul Dagallier.
the bud, velutinous outside, glabrous inside. Sepals 3, 8-13 mm long, 8-24 mm wide, imbricate to fused over up to ca. 30 % of their length, velutinous outside, glabrous inside, clear brown. Outer petals 3, 15-35 mm long, 13-23 mm wide, length:width ratio 1.1-2.2, broadly elliptic to elliptic, velutinous outside, gla- brous inside, cream outside, cream with a dark purplish red streak from base up to 75% of the petal length inside. Inner petals 3, 15-40 mm long, 9-16 mm wide, length:width ratio 1.5-2.7, obovate, valvate at apex, velutinous outside, glabrous inside, cream to cream with a dark purplish red streak at base up to 15% of their length outside, dark purplish red with cream apex inside. Stamens 1400 to 1600, 2.5-3 mm long, 0.4-1 mm wide, anthers linear, connective pro- longation truncate. Carpels 40 to 80, 3-4.5 mm long, 0.8-1.5 mm wide, pubes- cent, free; stigma 0.5 mm long, 0.8-1.1 mm wide, coiled, velutinous. Fruiting pedicel 10-20 mm long, 3-5 mm in diameter, velutinous. Monocarps 20 to 60, 24-90 mm long, 4.5-11 mm wide, length:width ratio 5-11, very narrowly cylindrical, torulose to torose, velutinous, greyish green; stipe 5-11 mm long, 1.5-3 mm wide, velutinous. Seeds 3-14 per monocarp, uniseriate, 3 to 9 mm long, 2-7 mm wide, ellipsoid.
Distribution. Endemic to Somalia-Masai Region: Kenya, Mozambique and Tanzania.
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1 es sl iD)
Figure 25. Uvariodendron gorgonis Verdc A young branch and apical ‘eragrostiform’ bud B flower, top view, and flower buds, side view C longitudinal section of flower bud D stamen, side view E carpel, side view F longitudinal section of carpel G fruit, side view H seed, side view. A from Verdcourt 1890 B-G from Drummond 1954 H from Verdcourt 3940 (type). Drawings by Heather Wood, from Verdcourt (1969; fig. 1, p. 514), Kew Bulletin 1969, © Board of Trustees of the Royal Botanic Gardens, Kew.
Habitat and ecology. Lowland to submontane secondary rain forests or semi-deciduous forest. Soil: coral rag or igneous intrusion. Altitude: 170- 950 ma.s.l.
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Latitude
Oo
20S
40S
60S
8S
10°S
1208
140$
16°S
J 4 { 4 @ @ Uvariodendron gorgonis vom fa 200 km -————4 250E 30°E 350E 400E 45°E Longitude
Figure 26. Distribution map of Uvariodendron gorgonis. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.
Phenology. Flowers collected from January to February and from July to No- vember. Fruits collected from January to March and from June to November.
Vernacular names. Tanzania: ‘Mtwamu’ (Mbago 1616).
Etymology. Although Verdcourt (1969) did not mention it in the protologue, the specific epithet might come from the Latin gorgonis (derived from the An- cient Greek gorgo). This refers to the gorgons, three creatures from the Greek mythology, depicted to have hairs made of living snakes. The name of Ud. gor- gonis might thus come from their fruits formed of long and numerous mono- carps, resembling a gorgon’s head.
Notes. This species differs from all other species by its fruits, unique in the genus. The fruits of Ud. gorgonis are composed of 20 to 60 monocarps, while most of the Uvariodendron species have fruits composed of 1 to 20 monocarps (except Ud. calophyllum and Ud. fuscum var. giganteum that have fruits com- posed of up to 35 monocarps). Moreover, the monocarps are 5 to 10 times longer than wide (vs. 1.3 to 4.5 times longer than wide in the other species). They are torulose to torose, i.e. very strongly constricted between the seeds. The ovules (and seeds) are uniseriate. The combination of these characters confers the fruits the aspect of a hairy head.
Vegetatively, this species is harder to differentiate as its leaves have dimen- sions that overlap with most of the other species. However, the bases of the leaves are quite peculiar: they appear generally acute to rounded but a closer look actually detects them as minutely decurrent at the extreme base. Similar- ly, the apices of the leaves are generally acute to acuminate, but can appear rounded to slightly retuse with a minute acumen.
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The fresh leaves of Ud. gorgonis also present a citrus smell when crushed, as in Ud. angustifolium, Ud. citriodorum and Uvariopsis citrata.
Preliminary conservation status. A previous assessment, that needs updat- ing, listed this species as Endangered EN under criteria B2ab(iii), based on its occurrence in eight locations in Tanzania (Eastern Arc Mountains & Coastal Forests CEPF Plant Assessment Project 2009a). Here, the EOO of this species is estimated at 203,044 km? and its AOO at 72 km”. It occurs in 11 locations in Tanzania, Kenya and Mozambique. Given its habitat is severely fragmented and there is continuing decline due to habitat loss and degradation (Eastern Arc Mountains & Coastal Forests CEPF Plant Assessment Project 2009a), it qual- ifies for the same previous status of Endangered EN under criteria B2ab(iii).
Additional specimens examined. KENYA - Coast + B. Verdcourt 1890 (k); Kwale District, Mrima Forest, Mrima Hill; 4°29'06.81'S, 39°15'47.19'E; 06 Sep. 1957 + B. Verdcourt 1911 (B, EA, K); Kwale District, Mrima Forest, Mrima Hill; 4°29'06.81'S, 39°15'47.19'E; 07 Sep. 1951 + J.RM. Brenan 14601 (EA, K, P); Kilifi District, K7, Kilifi District. Pangani ‘Kaya’ Forest; 3°51'S, 39°40'30'E; alt. 170 m; 19 Nov. 1978 « R.B. Faden 70/253 (K); Kwale District, Mrima Hill, about halfway betwee Mgambweni and Lungalunga; 4°29'S, 39°16'E; alt. 70 m; 25 Jun. 1970 S.A. Robertson MDE78 (K); Kwale District, Mrima Hill; 4°29'S, 39°16'E; alt. 270 m; 04 Feb. 1989. MOZAMBIQUE — Cabo Delgado + W.R.Q. Luke 9983 (MO), Qui- rimba NP, Ngura Inselberg; 12°51'S, 39°39'E; alt. 420 m; 10 Dec. 2003. TANZANIA — Lindi * FM. Mbago 2148 (kK), Ruawa Forest; 9°44'46.58'S, 39°33'04.77'E; alt. 250 m; 01 Sep. 2001 - Morogoro « A. Pécs 6061B (DSM); Morogoro Rural Dis- trict, Kimboza Forest Reserve, between Mkuyuni and Matombo; 7°00'S, 37°48'E; alt. 300 m; 19 Nov. 1969 « A. Pécs 6280F (DSM); Morogoro Rural District, Kim- boza Forest Reserve; 7°00'S, 37°48'E; alt. 300 m; 05 Nov. 1970 + B.J. Harris 3223 (DSM, EA); Morogoro Rural District, Kimboza Forest Reserve, KFR near Matombo, Uluguru Mts; 7°00'S, 37°48'E; 06 Sep. 1969 » C.D. Mgaza 323 (kK), Luzunguru forest reserve; 6°05'S, 37°40'E; 19 Sep. 1959 + F.C. Magogo 2171 (K); Morogoro Rural District, Kimboza Forest Reserve, Kibungo Forest Reserve (Kimboza); 7°00'S, 37°48'E; alt. 600 m; 31 Aug. 1981 » F.M. Mbago 1616 (DSM); Kilombero District, Lower Kihansi Hydropower Project; 8°24'S, 36°21'E; 30 Aug. 1997 * F.M. Mbago 1734 (K), T7: Udzungwa scarp, Upper Kihansi Gorge, forest opposite the spray zone; 8°34'54.77'S, 35°51'05.9'E; alt. 950 m; 15 Jul. 1998 « L.- P.M.J. Dagallier 47 (DSM, MPU, P WAG); Morogoro Rural District, Kimboza for- est; 7°01'16.89'S, 37°48'17.38'E; alt. 278 m; 15 Nov. 2019 + L.-PM.J. Dagallier 52 (DSM, K, MPU, P WAG); Morogoro Rural District, Kimboza forest; 7°01'18.69'S, 37°48'31.63'E; alt. 262 m; 15 Nov. 2019 » L.-PM.J. Dagallier 57 (DSM, MPU, P, WAG); Mvomero District, Turiani village; 6°09'36.19'S, 37°36'17.72'E; alt. 377 m; 18 Nov. 2019 + L.-PM.J. Dagallier 61 (DSM, MPU, P WAG); Mvomero Dis- trict, Turiani village; 6°09'46.83'S, 37°36'12.66'E; alt. 373 m; 18 Nov. 2019 + L.B. Mwasumbi 19144 (MO); Kilombero District, Kihansi gorge; 8°35'S, 35°51'50'E; alt. 800 m; 04 Sep. 1998 +