Uvariopsis dioica (Diels) Robyns & Ghesq., Ann. Soc. Sci. Bruxelles, Ser. B liii. 321 (1933)

Dagallier, Leo-Paul M. J., Mbago, Frank M., Couderc, Marie, Gaudeul, Myriam, Grall, Aurelie, Loup, Caroline, Wieringa, Jan J., Sonke, Bonaventure & Couvreur, Thomas L. P., 2023, Phylogenomic inference of the African tribe Monodoreae (Annonaceae) and taxonomic revision of Dennettia, Uvariodendron and Uvariopsis, PhytoKeys 233, pp. 1-200 : 1

Uvariopsis dioica (Diels) Robyns & Ghesq., Ann. Soc. Sci. Bruxelles, Ser. B liii. 321 (1933)

Figs 49F-M , 61 , 62

≡ Tetrastemma dioicum Diels, Bot. Jahrb. Syst. 38(3): 241 (1906). Type. Cameroon - Littoral • H.J.P. Winkler 909 (lectotype: B! (B 10 0153121), lectotype designated in Couvreur et al (2022), the specimen H.J.P. Winkler 908, cited in the protologue, was not found), Edea; 3°47'50"N, 10°07'50"E; Nov. 1904.

= Tetrastemma sessiliflorum Mildbr. & Diels syn. nov., Bot. Jahrb. Syst. 53(3-5): 440 (1915); ≡ Uvariopsis sessiliflora (Mildbr. & Diels) Robyns & Ghesq., Ann. Soc. Sci. Bruxelles, Ser. B liii. 322 (1933). Type. Cameroon - East Region • G.W.J. Mildbraed 5239 (holotype: B! (B 10 0153123); isotypes: BR! (BR0000008824233), HBG! (HBG502485)); Haut-Nyong, Lomié; 3°09'N, 13°38'E; 1911.

Description.

Tree to shrub 3.6-20 m tall, D.B.H 8-40 cm; young branches pubescent to glabrous, old branches glabrous. Petiole 1.9-5 mm long, 1-2.5 mm wide, pubescent to glabrous. Leaf lamina 111-245 mm long, 38-92 mm wide, length:width ratio 2.5-3.7, elliptic to obovate, base acute to rounded, apex acuminate, acumen 2-30 mm long, surface above glabrous, surface below glabrous; midrib impressed above, raised below, glabrous above, glabrous below; secondary veins 8-14 pairs, brochidodromous, impressed above, raised below; tertiary veins reticulate. Flowers unisexual, male and female flowers dimorphic, on same individuals (plant monoecious). Flower buds ovoid to conical, rarely globose. Male inflorescences borne in clumps, on thickenings of the trunk, mainly between the base and the lower 3 m of the trunk (but up to ca. 5 m on large specimens), composed of 5 to 20 flowers. Peduncle inconspicuous. Flower pedicel (4) 9-55 mm long, 1-1.5 mm in diameter, pubescent to glabrate. Bracts 1 at base and 1 towards the lower half of the pedicel, upper bract ca. 1 mm long, ca. 1 mm wide, broadly ovate, adpressed, semi clasping the pedicel, pubescent outside, glabrous inside. Sepals 2, 1.5-3 mm long, 2.5-5 mm wide, circular to broadly ovate, sparsely pubescent outside, glabrous inside, purplish brown. Petals 4, 6-17 mm long, 3.5-9.5 mm wide, length:width ratio 1.6-2.5, ovate to elliptic, free, valvate, pubescent to glabrous outside, glabrous inside, red to brownish red outside, yellowish cream to reddish at base inside. Stamens ca. 300, 0.2-0.5 mm long, 0.1-0.5 mm wide, anthers linear, connective prolongation truncate. Female inflorescences fewer in number than the male inflorescences, borne in clumps, on thickenings of the trunk, between the base and the lower 25-50 (150?) cm of the trunk, composed of 1 to 10 flowers. Flower pedicel (0) 20-77 (128) mm long, 1-2.5 mm in diameter, pubescent to glabrate. Bracts 1 to 3 at base and 1 to 2 towards the lower half of the pedicel, upper bract 1-3 mm long, 1-3 mm wide, broadly ovate, adpressed, semi clasping the pedicel, pubescent outside, glabrous inside. Sepals 2, 2-5 mm long, 4-11 mm wide, circular to broadly ovate, fused at base, sparsely pubescent outside, glabrous inside, purplish brown. Petals 4, 10-25 mm long, 6-17 mm wide, length:width ratio 1.2-2.5, ovate to elliptic, free, valvate (rarely fused at base over 1-3 mm), pubescent to glabrous outside, glabrous inside, red to brownish red outside, yellowish cream to reddish at base inside. Carpels 100 to 280, 1.5-3.5 mm long, 0.7-1.5 mm wide, pubescent, free; stigma 0-0.6 mm long, 0.5-1 mm wide, coiled. Fruiting pedicel 33-97 mm long, 1-3.5 mm in diameter, sparsely pubescent to glabrous. Monocarps, 1-5, 17-85 mm long, 10-50 mm wide, length:width ratio 1.2-2.1, ellipsoid to cylindrical, smooth, not ridged, sparsely pubescent to glabrous, pale brownish grey to yellow to red, sessile to shortly stipitate; stipe up to 3 mm long, 4-5 mm wide, glabrate. Seeds 5-8 per monocarp, biseriate, 15-22 mm long, ca. 15 mm wide, ellipsoid, in a translucid slimy pulp.

Distribution.

Endemic to Lower Guinean Domain of the Guineo-Congolian Region: Cameroon, Equatorial Guinea (Bioko island), Gabon, Nigeria, Republic of the Congo.

Habitat and ecology.

Lowland mature or old secondary rain forests. Altitude: 10-980 m asl.

Phenology.

Flowers collected from January to June and from October to December. Fruits collected from January to July and from October to November.

Notes.

Up. dioica resembles Up. guineensis , Up. pedunculosa and Up. solheidii in having elliptic to obovate leaves, with acute to rounded base and attenuate to acuminate apex. It differs from these species in having flowers borne in clumps of 5 to 20 flowers on thickenings of the trunk, lower than 3 m high (vs. inflorescences of 1 or 2 flowers). Up. dioica has 100 to 240 carpels, whereas all the other Uvariopsis species have less than 100 carpels. Only Up. korupensis and Up. pedunculosa can have up to 120 and 140 carpels, respectively, but Up. dioica has smaller leaves than Up. korupensis (11-25 cm long vs. 28-62 cm long) and smaller flower pedicels than Up. pedunculosa (20-77 mm long vs. 80-325 mm). Here we make Ud. sessiliflora synonym of Ud. dioica based on our phylogenetic analyses (Fig. 1 , Suppl. materials 1, 2). The specimen Mildbraed 5239, type of Ud. sessiliflora , has sessile female flowers. It represents an extreme in the variation of the flower pedicel, which might explain why it remained the sole representative of this name. Note that the authors of Ud. sessiliflora (as Tetrastemma sessiliflorum ) also already mentioned that the carpels of Mildbraed 5239 were similar to those of Ud. dioica ( Mildbraed and Diels 1915).

Preliminary conservation status.

The EOO of this species is estimated at 397,039 km2 and its AOO at 128 km2. Based solely on AOO, it would qualify for Endangered EN under the B2 criterion, but no other subcriterion (a, b or c) is met. Following IUCN criterion B, it is thus assigned a preliminary conservation status of Least Concern LC.

Additional specimens examined.

Cameroon - Central Region • G.W.J. Mildbraed 8260 (K), Übergangs - und Kampfgebiet gegen die Savanne an der Nord-grenze der Hylaea südlich des Sanaga zwischen Jaunde und Dengdeng unweit der vereinigung von Lom (Sanaga) und Djerem. Etwa 115 km N O Jaunde ; 4°33'04.96'N, 12°16'43.94'E; Mar. 1914 • H. Jacques-Félix 2493 (P), Ndiki; 4°46'N, 10°50'E; Nov. 1938 • P.R.J. Bamps 1458 (P), Résèrve forestière de Makak; 3°29'N, 11°01'E; 14 Dec. 1967 • R.G. Letouzey 12290 (K, P), Mambe près de Boga, 30 km N. Eseka. (feuille IGN 1/200 000 Edea ); 3°53'58.29'N, 10°46'58.4'E; 08 Dec. 1973 • R.G. Letouzey 9541 (MO, P, WAG, YA), Versant septentrional des Monts Mfiki au Sud de Ndo , 25 km NNE d'Esse; 4°19'N, 11°58'E; alt. 983 m; 09 Nov. 1969 - Littoral • R.G. Letouzey 12580 (P), Sude de Ngola (8 km Est de l'embouchure de la Sanaga); 3°33'55'N, 9°42'46'E; 05 Jan. 1974 • T.L.P. Couvreur 654 (WAG, YA), Mambe Massif, above Boga village, 100 km along road from Yaoundé to Edea ; 3°54'35.85'N, 10°46'25.97'E; alt. 686 m; 19 Jun. 2014 • T.L.P. Couvreur 659 (WAG, YA), Mambe Massif, above Boga village, 100 km along road from Yaoundé to Edea ; 3°54'26.07'N, 10°46'21.27'E; alt. 654 m; 20 Jun. 2014 - South Region • J.J.F.E. de Wilde 7754A (K, P, WAG), Roughly between the village of N'Kolandom and Station du Cacaoyer de N'Koemvone ; 2°48'N, 11°09'E; 27 Nov. 1974 • J.J.F.E. de Wilde 8270A (BR, MO, P, PRE, WAG), Station du Cacaoyer de N'koemvone, S. of Ebolowa, 14 km on the road to Ambam. On bank of the Seng river ; 2°49'N, 11°08'E; alt. 500 m; 05 Jun. 1975 • J.J.F.E. de Wilde 8709 (BR, MO, P, PRE, WAG, YA), Station du Cacaoyer de N'koemvone, S. of Ebolowa, 14 km on the road to Ambam. On bank of the Seng River ; 2°49'N, 11°08'E; alt. 550 m; 12 Dec. 1975 • R.G. Letouzey 4219 (K, P), Nkomo, près Ngoassé au S; de la rivière Lobo - feuille IGN 1/200000 Akonolinga ; 3°14'N, 12°04'E; 13 Feb. 1962 • R.G. Letouzey 4230 (P), Nkomo, près Ngoassé au S; de la rivière Lobo - feuille IGN 1/200000 Akonolinga ; 3°14'N, 12°04'E; 14 Feb. 1962 • R.G. Letouzey 9934 (K, P), près de la rivière Mboro, près Mevous, 50 km SE d'Ebolowa sur piste d'Evindissi ; 2°36'N, 11°28'E; 30 Jan. 1970 - South-West Region • G.W.J. Mildbraed 10647 (K), Bibundi-Pflanzung, Westlich des Kamerunberges ; 4°12'N, 8°59'E; Nov. 1928 • J.F. Villiers 2429 (P), Pente SW Mt Cameroun, NE Bakingili, 20 km WNW Limbe ; 4°05'22.16'N, 9°05'21.91'E; alt. 800 m; 09 Dec. 1984 • J.J. Wieringa 2029 (BR, E, FHO, K, MO, SCA, WAG); Fako , Limbe, W of Njonji Lake; 4°08'N, 9°01'E; alt. 150 m; 27 Jan. 1994 • M.R. Cheek 5482 (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' ; 4°08'N, 9°01'E; alt. 300 m; 18 Nov. 1993 • M.R. Cheek 5501 (K, MO, 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' ; 4°08'N, 9°00'E; alt. 5 m; 19 Nov. 1993 . Equatorial Guinea - Bioko Sur • W.R.Q. Luke 11970 (EA, MA), Moaba - Moka Trail Pt 139 - Pt 138; 3°17'26.92'N, 8°38'29.83'E; alt. 650 m; 16 Mar. 2007 • W.R.Q. Luke 13050 (MA), Ureka pt 330 to Moraka pt 339; 3°15'19.08'N, 8°35'04.56'E; alt. 141 m • W.R.Q. Luke 13113 (EA, MA, MO), Badja E Trail pt 338; 3°18'04.68'N, 8°31'01.2'E; alt. 700 m; 21 Jan. 2009 . Gabon - Moyen-Ogooué • E. Bidault 1558 (BR, BRLU, LBV, MO, P, WAG), Est du lac Azingo, à 30 km au Nord-Ouest de Lambarene ; 0°30'32.42'N, 10°05'08.01'E; alt. 48 m; 08 Jun. 2014 • O.L.S. Lachenaud 2064 (MO), piste du lac Azingo, ± 10 km au NE du lac et 30 km au NW de Lambrene ; 0°28'41'N, 10°01'59'E; alt. 20 m; 25 Oct. 2014 • T.L.P. Couvreur 926 (LBV, WAG, YA), 27 km after Lambaréné, on road to Bifoum (N1), then around 20 km on road to Lake Azingo ; 0°29'38.73'N, 10°01'55.24'E; alt. 23 m; 24 Nov. 2015 • T.O.B.E.B. Stévart 4792A (P, WAG), Okala, North of Libreville. Terrain de Montigny à Okala ( Libreville ); 0°29'N, 9°25'E; alt. 10 m; 12 Feb. 2014 - Ogooué-Ivindo • A. Hladik 1472 (BRUNOY, P, P, US), Ipassa, au croisement des layons J et VII; 0°30'N, 12°48'E; alt. 490 m; 29 Oct. 1971 • J.M. Reitsma 3507 (LBV, MO, WAG), Primary rain forest, near village Ekobakoba , 50 km SE of Makokou; inventory; 0°23'N, 13°06'E; 21 May. 1987 • L.J. Dorr 4248 (LBV, MO), Station I.R.E.T. (M'Passa Field Station). 10 km S de Makokou sur la riviere Ivindo ; 0°30'N, 12°45'E; alt. 500 m; 13 May. 1985 • L.J. Dorr 4275 (LBV, MO, P), Station I.R.E.T. (M'Passa Field Station), 10 km S de Makokou sur la riviere Ivindo ; 0°30'N, 12°45'E; alt. 500 m; 14 May. 1985 • M.S.M. Sosef 2210 (BR, LBV, MO, WAG), Ipassa Reserve, IRET Research Station , SW of Makokou; 0°31'N, 12°48'E; alt. 350 m; 04 Nov. 2005 - Woleu-Ntem • A.M. Louis 4098 (BR, LBV, MO, WAG), 25 km NE of Bitam, Nsimy ; 2°08'N, 11°22'E; 02 May. 1995 . Nigeria - Edo State • A.F. Ross 2/6 (K) ; Benin, Sapoba Forest Reserve; 6°06'N, 5°53'E; 1934 • B.O. Daramola FHI72315 (K, MO), Iyekoriowon. Forest Reserve. In P.S.P. 82 Ugo ; 6°05'19.05'N, 6°00'04.46'E; 04 Oct. 1973 • R.D. Meikle 628 (K, P), Usonigbe Forest Reserve near Sapoba ; 5°56'17.52'N, 5°53'20'E; 16 Nov. 1944 • R.W.J. Keay FHI28066 (K, K, P) ; Benin, Sapoba Forest Reserve , Compte. 9, S.S. I; 6°06'N, 5°53'E; 03 Nov. 1950 - Kogi State • M.G. Latilo FHI47768 (K); Kabba, Southern Adoru Forest Reserve, Igala, bank of river Owe near Adoru ; 6°55'38.49'N, 7°05'38.55'E; 01 Jul. 1963 . Republic of the Congo - Pool • J. Koechlin 4001 (P), Bangou, Forêt de; 3°54'S, 14°27'E; Dec. 1956 • P. Sita 3264 (P), Forêt de Bangou, Est de M'Passa ; 4°29'34'S, 14°45'28'E; 18 Dec. 1971 .

Figures

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 Asteranthe asterias (Dagallier 10) D Hexalobus crispiflorus (no specimen associated) E Uvariastrum zenkeri (no specimen associated) F Isolona hexaloba (no specimen associated) G I. 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 97 b) R Up. bakeriana (Couvreur 1000) S Up. submontana (Couvreur 627) T Up. pedunculosa (Couvreur 878). Photos CC BY-NC 4.0 A, D-F, J, N, O, Q-T Thomas Couvreur B, C, G-I, L Leo-Paul Dagallier K Carel Jongkind M Ehoarn Bidault P Olivier Lachenaud.

Figure 49. Uvariopsis bakeriana (Hutch. & Daltz.) Robyns & Ghesq A leaf, top view B detail of female flower, two petals removed C petal, inner view D carpel, side view, front view and detail of ovules E monocarp Uvariopsis dioica (Diels) Robyns & Ghesq F leaf, top view G male flowering pedicels and flowers H detail of male flower, two petals removed I stamen J female flowering pedicel K detail of female flower, all four petals removed L carpel, front view and detail of ovules M fruits. A-E from Brenan 9409 F-L from Keay 28066 M from Letouzey 4230. Drawings by Helene Lamourdedieu, Publications Scientifiques du Museum national d'Histoire naturelle, Paris.

Figure 61. Uvariopsis dioica (Diels) Robyns & Ghesq. Fries A trunk with infrutescences B leaves, upper side C leaves, lower side D clump of inflorescences on the trunk E detail of semi-open female flower, side view F fly on petal of femal flower G male flower, top view H detail of female flower, top view (left) and bottom view (right) I transversal cut of fruit J detail of fruit, side view K fruits mature (right) and unripe (left), top view. A, I-K Couvreur 654 B, C Lachenaud 2064 D, G Stevart 4792 A E, F, H Bidault 1558. Photos A, I-K Thomas Couvreur B, C Olivier Lachenaud (CC BY-NC-ND 3.0) D, G Tariq Stevart (CC BY-NC-ND 3.0) E, F, H Ehoarn Bidault (CC BY-NC-ND 3.0).

Figure 62. Distribution map of Uvariopsis dioica. Shades of grey represent elevation, from white (sea level) to darker grey (higher elevation). The inset shows the extent of the map over Africa.