Taxonomic studies of Diospyros (Ebenaceae) from the Malagasy region. V. Synoptic revision of the Bernieriana group in Madagascar and the Comoro Islands

Abstract Schatz, G.E., P.P. Lowry II & P.B. Phillipson (2020). Taxonomic studies of Diospyros (Ebenaceae) from the Malagasy region. V. Synoptic revision of the Bernieriana group in Madagascar and the Comoro Islands. Candollea 75: 203–218. In English, English and French abstracts. A synoptic revision of the Bernieriana group of Diospyros L. (Ebenaceae) in Madagascar and the Comoro Islands is presented in which seven species are recognized, including four new species that are described and illustrated (Diospyros hongwae G.E. Schatz, Lowry & Phillipson, Diospyros ranirisonii G.E. Schatz, Lowry & Phillipson, Diospyros silicea G.E. Schatz, Lowry & Phillipson, and Diospyros suarezensis G.E. Schatz, Lowry & Phillipson). A key to the species is provided, along with a risk of extinction assessment for each species using the IUCN Red List criteria. Two species are assessed as “Endangered” (Diospyros hongwae and Diospyros silicea), one as “Vulnerable” (Diospyros ranirisonii), two as “Near Threatened” (Diospyros suarezensis and Diospyros torquata H. Perrier), and two as “Least Concern” (Diospyros bernieriana (Baill.) H. Perrier and Diospyros danguyana H. Perrier).


Introduction
An ongoing revision of the Ebenaceae of Madagascar, undertaken to update the Flore de Madagascar et des Comores treatment by Perrier de la Bâthie (1952b), has revealed a large number of undescribed species in the genus Diospyros L. (Schatz & Lowry, 2011, 2018Schatz et al., 2013;Madagascar Catalogue, 2020). Currently, of the c. 730 accepted species of Diospyros worldwide (Govaerts, 2020), 97 species are recognized in Madagascar, of which all but three species are endemic, and an additional 154 endemic species have been tentatively identified as new to science (Madagascar Catalogue, 2020). Most Malagasy Diospyros species can easily be placed in one of about a dozen informal morphological groups recognized on the basis of vegetative and reproductive features. Such groups constitute hypotheses of monophyletic groups within Diospyros as revealed by analyses using molecular sequence data (Duangjai et al., 2006(Duangjai et al., , 2009Linan et al., 2019). One such group, comprising Diospyros bernieriana (Baill.) H. Perrier and its putative relatives, has been named the Bernieriana group. It is characterized by axillary, solitary female flowers with a cupuliform to cylindrical-tubular to obconical calyx with an entire, truncate or sometimes shallowly lobed apex, the calyx strongly accrescent in fruit such that the fruit is usually wholly included within the calyx (the exceptions being D. hongwae G.E. Schatz, Lowry & Phillipson and D. silicea G.E. Schatz, Lowry & Phillipson in which the apex of fruit is visible and slightly exserted above the calyx), and the calyx irregularly tearing and breaking off during fruit maturation.
Three currently recognized species conform to the Bernieriana group (D. bernieriana, D. danguyana H. Perrier, and D. torquata H. Perrier), to which an additional four new species are herein described, each accompanied by an illustration and an assessment of its conservation status according to the IUCN Red List Categories and Criteria (IUCN, 2012). Because three of the species treated in this revision can form sufficiently large trees to be potential sources of ebony wood, which is under significant pressure in Madagascar from illegal, unsustainable exploitation (Mason et al., 2016), geo-coordinates and detailed locality data have been withheld for them, and public access to this information through the Madagascar Catalogue (2020) has been restricted. Full specimen records and distribution maps are available for the remaining members of the group in the Catalogue of the Plants of Madagascar (Madagascar Catalogue, 2020), and can also be found in the Sonnerat (2020) database. Post-facto georeferencing of historical specimens is indicated by square brackets.  Distribution and ecology. -Diospyros bernieriana is known from dry to subhumid forest on both sand and calcareous substrates from Oronjia south to Vohemar along the east coast of Madagascar and Mahajanga along the west coast, as well as from Mayotte, Mwali and Grande Comore (Madagascar Catalogue, 2020), at an elevation of 0 -432 m.

Key to the species of the Bernieriana group of Diospyros
Conservation status. -Diospyros bernieriana has a geographic range in the form of an Extent of Occurrence (EOO) of 188,912 km2 and a minimum Area of Occupancy (AOO) of 148 km2. It is present in the Andrafiamena Andavakoera, Ankarana, Antrema, Loky Manambato, Montagne des Français, and Oranjia protected areas. Outside of protected areas, it is threatened by fire, forest clearing for agriculture, grazing, and exploitation for firewood and house construction material. With respect to the principal threat of forest clearing for agriculture, it exists at 35 locations. Therefore, D. bernieriana can be assessed for its risk of extinction as "Least Concern" [LC].
Notes. -Diospyros bernieriana is one of only three Malagasy members of the genus that are not endemic to the island (Madagascar Catalogue, 2020). It is characterized by leaves with distinctly undulate margins and a calyx in fruit that completely encloses the fruit (Fig. 1A).
Two sheets of Bernier 259 are deposited in the Paris herbarium, one of which is annotated "Olax bernieriana H. Bn." in Baillon's hand, which we take to be the holotype. A second sheet of Bernier 259 with the original label is a mixture, comprising a small branch of D. bernieriana and a second branch that is clearly assignable to D. haplostylis Boivin ex Hiern. This sheet has an annotation label prepared by Perrier de la Bâthie indicating that he assigned it to D. haplostylis var. hildebrandtii, and indeed he cited Bernier 259 under that name. In order to avoid any possible confusion, we have therefore annotated the material belonging to D. bernieriana as Bernier 259 ' A' and that to D. haplostylis as Bernier 259 'B'. The holotype of D. hildebrandtii at B was destroyed. We have therefore selected the best preserved of the two sheets at P as the lectotype.   Described from the northwestern portion of the overall range of D. danguyana, and thus from the transition from subarid to dry bioclimates, M. enervis exhibits leaves that are somewhat less strongly revolute upon drying, but are otherwise identical to D. danguyana in shape and size, with identical fruit completely enclosed within the cylindrical-tubular accrescent calyx. Diospyros danguyana can be distinguished from other members of the Bernieriana group by its linear leaves 4 -8 times longer than wide, its elliptic to subspherical female flowers only slightly longer than wide, and its distinctly lobed accrescent calyx enclosing the fruit, the lobes 3 mm long.   Shrub to tree 4 -15 m tall. Young stems initially sparsely to moderately densely covered with appressed, very short (< 0.1 mm) gray trichomes, glabrescent. Leaves 4 -12 × 1.4 -4.9 cm, elliptic, glabrous above and below, glossy above, base acute to cuneate, margin flat (weakly undulate in fresh material), apex acuminate, the acumen to 11 mm, rounded, midrib slightly impressed above, raise below, venation weakly brochidodromous with 8 -10 secondary veins per side, flat to slightly raised above and below, faintly visible, tertiary venation indistinct; petiole 7 -11 mm, 1 mm diam., canaliculate, initially sparsely to moderately densely covered with appressed, very short (< 0.1 mm) gray trichomes glabrescent. Male flowers not seen. Female flowers solitary in the axils of leaves and fallen leaves; pedicel 2 -3 mm long, 2 -3 mm diam., bearing several bracts (based upon bract scars), densely covered with very short, erect, light golden to gray trichomes; flowers ellipsoid at anthesis, calyx fully fused, adnate to the receptacle, the apex entire, 7 -8 mm long, 6 mm in diam., glabrous outside, densely covered with very short, erect light golden to gray trichomes inside; calyx rapidly expanding post anthesis, extending an additional 4 mm, cupuliform; corolla tubular, 15 mm long, 4 mm in diam., lobes 4, ovate, 5 × 4 mm, apex acute, adaxially concave, densely covered with very short, appressed trichomes outside, glabrous inside; staminodia c. 18, inserted at base of corolla tube, filaments 3 mm, the distal 1 mm free, antherodes 1.5 mm, ovary subspherical, crowned by conical style, the stigma 4-lobed, lobes 1.5 mm long. Pedicel in fruit expanding to 4 -5 mm in diam., with a distinct apical rim to 6 mm in diam., the apex convex. Receptacle in fruit to 3 mm thick at base. Fruit subspherical, the apex slightly exserted above the prolonged cupuliform calyx, i.e., visible, c. 10 -12 mm in diam., densely covered with short (c. 0.5 mm), appressed, light golden trichomes, crowned by the style/stigma remnant, cone-shaped, 2 -4 mm tall, 2 mm in diam. at base, densely covered with shorter (c. 0.2 mm) semi-appressed darker golden trichomes.

Diospyros danguyana
Etymology. -The species epithet honors our colleague and good friend Cynthia Hong-Wa, who brought order to the large and complex genus Noronhia Stadtm. ex Thouars (Oleaceae). Conservation status. -Diospyros hongwae has a restricted geographic range in the form of an EOO and AOO of 0.263 km2. It is not known from within any protected area, and is threatened by forest clearing for agriculture, grazing, fire, and exploitation for firewood and construction material, all of which are projected to result in continuing decline. With respect to the principal threat of forest clearing for agriculture, it exists at two locations. Therefore, D. hongwae can be assessed for its risk of extinction as "Endangered" [EN B1ab(i,ii,iii,iv,v)+2ab(i,ii,iii,iv,v)]. Notes. -The collections Humbert & Capuron 25932 and Service Forestier 3075 represent a single gathering divided between two separate collection series. Diospyros hongwae can be distinguished from other members of the Bernieriana group by its large leaves with flat margins (weakly undulate in fresh material) and its subspherical fruit, the apex of which is slightly exserted above the prolonged cupuliform calyx and thus visible.

Holotypus: Madagascar. Region Atsimo-Andrefana
Etymology. -The species epithet refers to the weathered siliceous sand substrate where the new species occurs.
Distribution and ecology. -Diospyros silicea is known from only two gatherings in subarid forest and thicket on siliceous sand from Zombitse-Vohibasia National Park south to Tsiombe (Madagascar Catalogue, 2020), at an elevation of 250 -850 m.
Conservation status. -Diospyros silicea has a restricted geographic range in the form of an AOO of 8 km2. It is present from the Zombitse-Vohibasia National Park. At its other known locality, east of Tsiombe, it is threatened by grazing, fire, and exploitation for firewood and construction material, all of which are projected to result in continuing decline. With respect to the principal threat of grazing, it exists at two locations. Therefore, D. silicea can be assessed for its risk of extinction as "Endangered" [EN B2ab(iii)].   Shrub to tree 1.5 -5 m tall. Young stems densely covered with erect, very short (< 0.1 mm) gray trichomes. Leaves 0.8 -2.7 × 0.3 -1.6 cm, elliptic to obovate, glabrous and glossy above, glabrous or initially with white farinose indumentum and then glabrescent below, base acute to obtuse, margin revolute to strongly revolute and then obscuring much of the abaxial lamina surface, apex obtuse to rounded, the very tip rounded, midrib flat to slightly impressed above, slightly raised below, venation weakly brochidodromous with 3 -4 secondary veins per side, flat to slightly raised above, only faintly visible above and below, tertiary venation indistinct; petiole 1 -3 mm, 0.8 mm diam., canaliculate, densely covered with erect, very short (< 0.1 mm) gray trichomes. Male flowers not seen. Female flowers solitary in the axils of leaves and fallen leaves; pedicel 0.5 -1 mm long, 0.7 mm diam., bearing several bracts densely covered with very short, appressed, light golden to gray trichomes; flowers obconical at anthesis, calyx fully fused, obconical, 4 -5 mm long, 2 mm diam. at base to 3 -3.5 mm in diam. at apex, the apex entire, densely covered with rufous farinose trichomes and very short, appressed light golden to gray trichomes outside, very densely covered with very short semi-appressed light golden trichomes inside, glabrescent outside; calyx rapidly expanding post anthesis, extending an additional 4 -9 mm, with visible venation, the apex entire; corolla tubular to slightly obconical, 5 mm long, 2 mm in diam. at base to 2.5 mm diam. at apex, glabrous for basal 2/3, densely covered with very short appressed trichomes for apical 1/3, lobes 3 or 4, broadly ovate, 2.5 × 2 mm, apex obtuse, densely covered with very short, appressed trichomes outside, glabrous inside; staminodia 4, inserted toward the apex of corolla tube, filaments adnate to corolla, 3 mm, the, antherodes 1 mm, ovary obovoid to subspherical, 2 mm tall, 2 mm in diam., densely covered with short appressed trichomes, crowned by the cylindrical style, 2 mm tall, 0.5 mm diam., densely covered with short appressed trichomes. Pedicel in fruit expanding to 2 mm long, 3 -5 mm in diam. Fruit 9 -12 mm in diam., subspherical, initially enclosed within the prolonged calyx until it breaks off, densely covered with short (c. 0.5 mm), appressed, light golden trichomes toward the apex, crowned by the style/stigma remnant, narrowly cone-shaped, 2 mm tall, 0.8 mm in diam. at base. Distribution and ecology. -Diospyros suarezensis is known from dry forest on sand in the DIANA region from Oronjia south to Irodo (Madagascar Catalogue, 2020), at an elevation of 0 -280 m.

Notes
Conservation status. -Diospyros suarezensis has a restricted geographic range in the form of an EOO of 439 km2 and a minimum AOO of 68 km2. It is present in the Ambodivahibe Marine Reserve and Oronjia protected areas. Outside of protected areas, it is threatened by grazing, fire, and exploitation for firewood and construction material, all of which are projected to result in continuing decline. With respect to the principal threat of fire, it exists at 16 locations. Therefore, D. suarezensis can be assessed for its risk of extinction as "Near Threatened" [NT], as it nearly qualifies as "Vulnerable" under Criteria B1 and B2 (IUCN, 2012).
Notes. -Diospyros suarezensis can be distinguished from other members of the Bernierana group by its small elliptic to obovate leaves with revolute margins, and its subspherical fruit enclosed within the accrescent calyx lacking lobes.