A revision of Ziziphus (Rhamnaceae) in Borneo

The genus Ziziphus (Rhamnaceae) is revised for Borneo. 13 species are recognised using morphological evidence, including three new endemic species: Ziziphus cuspidata, Z. domatiata and Z. puberula. Borneo is therefore the island with the greatest known diversity of Ziziphus species. The area surrounding Mount Kinabalu is particularly diverse, with nine species occurring in Ranau. Two new varieties of Z. borneensis are also described here, Z. borneensis var. ranggam and Z. borneensis var. velutina, five new synonyms are established, including the placement of Z. elmeri as a synonym of Colubrina beccariana. A taxonomic treatment, including a preliminary IUCN conservation status assessment, is presented for each species and variety.


Introduction
Ziziphus Mill. is a genus in the Rhamnaceae of about 80 species of deciduous and evergreen shrubs, climbers and trees occurring throughout the Old World (OW) tropics, subtropics and warmer temperate regions (Hauenschild et al. 2016;Medan & Schirarend 2004;POWO 2019). Leaves are typically triplinerved, stipules spinose, inflorescences cymose and fruits drupaceous (Medan & Schirarend loc. cit.). The fruits of almost all species could be edible (Latiff 1991), and jujube (Ziziphus jujuba Mill.) and ber (Z. mauritiana Lam.) are grown commercially. The genus was included in the morphologically heterogeneous Zizipheae Brongn. (Brongniart 1843, as "Zizypheae") by Hooker (1862), Weberbauer (1895) and Suessenguth (1953). Zizipheae however is predated by Paliureae Reiss. ex Endl. as noted by Schirarend & Olabi (1994), which is the currently accepted name for the tribe that includes Ziziphus. An analysis of rbcL and trnL-F sequence data by Richardson et al. (2000) confirmed the placement of Ziziphus into Paliureae. Morphological differences between Old World (OW) and New World (NW) species had been reported by several authors (listed by Islam & Simmons 2006) and an analysis of ITS, 26S rDNA and trnL-F data by Islam & Simmons (op. cit.) revealed that the genus was not monophyletic, with OW and NW species belonging to separate lineages. An additional analysis of trnL-F and ITS sequence data by Hauenschild et al. (2016) further supports that the genus Ziziphus as previously defined is not monophyletic and NW species have subsequently been reattributed to the genera Sarcomphalus P.Browne in Paliureae and Pseudoziziphus Hauenschild (op. cit.) in Rhamneae Hook.f. emend. J.E.Richardson (Richardson et al. 2000).
Ziziphus is found across diverse habitats, from savanna-adapted species such as Z. mucronata Willd., widely distributed in the grasslands of Africa (GBIF 2019), to rainforest endemics like most of the species studied here. The genus displays a range of morphological adaptations to these environments: spiny shrubs occurring in xeric shrublands such as Z. spinachristii (L.) Desf. (GBIF 2019), unarmed rainforest trees to 25 m tall such as Z. angustifolia (Miq.) Hatus. ex Steenis, widely distributed in South-East Asia, and armed rainforest woody climbers like most species studied here. Whether functional traits reflect habitat adaptations is part of ongoing work, in particular whether traits such as spinescence reflect a response adaptation to a biome or have facilitated entrance into the biome (Rickenback et al. in prep.). The centre of both the distribution and evolution of Ziziphus seems to be SE Asia (Liu & Cheng 1995); c. 50 species occur in Asia as opposed to c. 15 in Africa (GBIF 2019). Preliminary genus-level studies also suggest the origin of the genus may have been Asian (Rickenback et al. in prep.). This is consistent with the conclusions of Richardson et al. (2004) who also noted good representation of sister taxa in the Late Eocene-Miocene of North America and Eurasia, suggesting a Laurasian origin for this group followed by more recent migration to Africa. Despite being widely distributed, questions remain around the age, dispersal and morphological adaptations of the genus. Ziziphus is especially diverse in Malesia with over 25 currently accepted species (POWO 2019). Most of the c. 15 SE Asian genera of Rhamnaceae have yet to be revised, although a synopsis of Smythea (Cahen & Utteridge paper (Appendix 1). Material was examined under a Zeiss Stemi 1000 binocular microscope at magnifications of up to ×350. Leaf anatomy terms used are from Hickey (1979). Hair density terms are defined as follows: sparse when hairs are scattered enough not to touch when pressed towards each other, abundant when hairs are close enough to touch if pressed towards each other, dense when hairs are so close to each other that they hide the surface of the organ they grow on. Other morphology terms follow Beentje (2010). Measurements were made on material available at K and for specimens collected in Borneo only, except for type specimens of species occurring there but collected outside the island. To facilitate species identification, average measurements are sometimes used in the Key to species. Averages were calculated by recording measurements in spreadsheets and excluded the least developed, distal leaves. Habitat, elevation, vernacular names and phenological information are also indicated here for Borneo records only; and only specimens from Borneo are listed in the specimens examined. Habitat names used are from Ecoregions 2017 (Dinerstein et al. 2017). Collection locality coordinates used for species distribution maps were retrieved from label information for Borneo specimens and from GBIF (2019) for specimens collected outside the island. GeoCat (Bachman et al. 2011) was used to calculate Extents of Occurrence (EOO) and protected areas were located using the World Database on Protected Areas online interface (IUCN & UNEP-WCMC 2019). smallest leaves are in Z. havilandii, usually 2. 5 -5.5 cm), the presence of many dark glands, appearing as black spots, covering the abaxial surface (present in Z. havilandii and Z. suluensis, absent in all other species), the number of strong veins branching off the outer main veins towards the leaf margin (absent in Z. calophylla, Z. havilandii and Z. suluensis; c. 4 on either side in Z. domatiata, c. 5 in Z. cumingiana var. cumingiana, c. 6 in Z. cuspidata and Z. horsfieldii, c. 8 in Z. borneensis except > 15 in var. ranggam, > 10 in Z. puberula, > 20 on either side in Z. angustifolia, Z. crebrivenosa, Z. kunstleri and Z. ridleyana) and the presence of hairs on the abaxial lamina surface, main veins excluded (hairy in Z. borneensis, Z. cumingiana var. cumingiana, Z. cuspidata, Z. crebrivenosa, Z. kunstleri and Z. ridleyana vs glabrous to subglabrous in other species). The prominence, closeness and branching of transverse veins provide additional characters for identification (e.g. clearly raised, spaced by c. 5 mm from each other and often branching in Z. kunstleri; barely raised, spaced by c. 1 mm from each other and unbranched in Z. calophylla).

Inflorescences and flowers
All Borneo Ziziphus species present a typical Rhamnaceae flower, with five valvate, adaxially keeled calyx lobes, five small hooded petals each enclosing a stamen, and a fleshy nectar disk (Fig 2G & Fig. 4G). In the Ziziphus of Borneo, the disk surrounds a partially immersed ovary and is 10-pitted ( Fig. 2H & Fig. 4H), except in Z. angustifolia and Z. ridleyana where the disk is rugose and appears ± 20-pitted. Ziziphus angustifolia and Z. ridleyana flowers also differ in having 2 -4 style arms vs 2 in all other species. These flower characters, along with the unarmed tree habit (all other species in Borneo are spiny climbers), could indicate that the two species are in a separate clade. Otherwise, flowers appear relatively consistent morphologically. They are arranged in cymes, which can either be subsessile and almost fascicle-like (in Z. angustifolia, Z. borneensis, Z. cumingiana and Z. ridleyana) or clearly pedunculate (all other species) ( Fig. 2F & Fig. 4F). Ziziphus kunstleri is distinctive in the leaves subtending the cymes being distinctly smaller and narrower than other leaves, falling soon, and the inflorescences ultimately appearing to be arranged in panicles. Leaves subtending the cymes also tend to fall soon in Z. calophylla and Z. suluensis but they are not morphologically distinct from other leaves; the leaves subtending the cymes seem more or less persistent in all other species. Bracteoles at the base of pedicels are present and are narrowly triangular, entire to laciniate and 1 -5 mm long (Fig. 2F).

Fruit
Fruits are particularly useful for the identification of Ziziphus species in Borneo and provide the most diagnostic characters along with the leaves. All are single-stoned and fleshy (drupes), but they vary in size, shape and pubescence. Those of Ziziphus crebrivenosa are unique in being covered in raised, blister-like lenticels. Ziziphus cumingiana is recognised in the small fruits, c. 7 mm long (vs at least 10 mm long in all other Borneo Ziziphus species). Only three species have glabrous fruits: Z. cumingiana, Z. cuspidata (Fig. 2L) and Z. domatiata (Fig. 3E). Ziziphus horsfieldii fruits are characteristically obovoid (wider towards apex) and c. 1.1 × 1.1 cm. Except for Z. crebrivenosa, which has fruits with raised lenticels, Z. borneensis and Z. puberula are the only other species of the genus in Borneo with fruits that are ellipsoid, > 1.5 × longer than wide, and > 2 cm long (vs globose to obovoid, < 1.5 × longer than wide, or, if ellipsoid, then < 2 cm long) (Fig. 4J).
paniculate; pedicels and outside of flowers abundantly to densely hairy. Fruits 1 -3 cm long, globose, obovoid or ellipsoid, glabrous to densely hairy .  Merrill (1905), is selected as the lectotype rather than the US one because Merrill worked in NY; sheets of Forbes 910, the only collection mentioned by Baker (1923), are available in several institutions and the BM material is selected as the lectotype because it was the most likely to have been examined by Baker.

Ziziphus borneensis
Merr. (Merrill 1929: 178). Type: Malaysia, Sabah, Sandakan, Oct. -Dec. 1921 Woody climber to at least 20 m long; girth to at least 6 cm in diam., spiny. Branchlets terete, with longitudinal striations and visible lenticels when surface not hidden by indumentum, sparsely to densely hairy on young parts and distal portions, becoming sparsely hairy to glabrous when mature, hairs variable, usually c. 0.5 mm long, often > 1 mm long, straight to curved, spreading to appressed, reddish. Stipules paired on very young shoots, one becoming a persistent recurved spine, (2 -) 3 (-5) mm long, the other short-lived, entire, ovate, c. 4 × 2 mm, hairs dense. Leaves discolorous, drying greenish-brown, blade slightly asymmetric, narrow ovate (-ellipticoblong), (3.6 -) 7 (-15.0) × (1.4 -) 3 (-5.3) cm, chartaceous to subcoriaceous, apex (acute -) attenuate (-acuminate), base (obtuse -) rounded (-subcordate), often weakly oblique, margins entire (-finely serrate), with minute callosities that dry much darker than the lamina, > 150 on either side, often protruding and c. 0.1 mm long, margin slightly thickened, hairs usually present along margin; primary veins 3, impressed adaxially, raised abaxially, hairs along primary veins dense on either side of lamina, c. 0.4 mm long, mostly antrorse, reddish; strong marginal veins coming off the outside of the two outer main veins c. 8 on either side (except > 15 in var. ranggam), ascending and ending in a distinct intramarginal vein running along the leaf margin (except indistinct in var. kinabalui and var. velutina), angle of divergence with outer main veins c. 45°; transverse veins between the main veins conspicuous, coming off midrib at c. 90°, raised, spaced by c. 1 mm from each other, usually unbranched, straight (scalariform); higher order reticulations between transverse veins usually barely discernible (except reticulate abaxially, with the longitudinal venules between the transverse veins that join the main veins conspicuous and raised in var. ranggam); lamina subglabrous to densely hairy, always at least hairy along main and transverse veins, soft to touch when densely hairy, hairs c. 1 mm long, spreading to curved-antrorse, reddish; no domatia visible; petiole slightly dorsiventrally flattened, (2 -) 4 (-6) mm long, hairs dense, indumentum extending to widened base of main veins adaxially. Inflorescence of axillary, subsessile fascicle-like cymes, 2 -8 (-10) flowers in each cyme; peduncles rudimentary, rarely developed to 4 mm long; pedicels to 4 mm long, hairs dense, reddish, c. 0.5 mm long, mostly spreading to patent; bracteoles entire, narrowly triangular, c. 2 mm long, hairy. Flower hypanthium densely hairy on the outer surface, hairs c. 1 mm long, appressed-antrorse, reddish; sepals triangular, 1.5 -3 mm long, greenish when fresh, glabrous and keeled adaxially; petals clawed, c. 2.5 mm long, obcordate, white when fresh; stamen filaments flat, subulate, c. 2 mm long, pale yellow-green when fresh, anthers c. 0.5 mm long, enclosed by petals; nectary disk pentagonal, weakly 10-pitted, glabrous, style arms 2, free for c. 1 mm long, strongly diverging, glabrous; ovary partially immersed, hairs dense. Fruit a drupe, ripening greenish-yellow to red, c. 2.2 × 1.5 cm, ellipsoid, surface wrinkly when dry, covered in minute reddish hairs < 0.1 mm long; fruiting pedicels curved, c. 5 mm long, hypanthium remains caving in at base of fruit. Branchlets sparsely to densely hairy on young parts and distal portions, hairs variable, usually c. 0.5 mm long, spreading to appressed. Leaves narrow ovate (-ellipticoblong), (3.6 -) 7 (-11.4) × (1.4 -) 3 (-4.9) cm; callosities protruding off a margin that is usually entire in outline; strong marginal veins coming off the outside of the two outer main veins c. 8 on either side, ascending and ending in a distinct intramarginal vein running along the leaf margin. Higher order reticulations between transverse veins barely discernible; lamina densely hairy abaxially on its entire surface.  1B), the outline of the margin, which is entire (vs serrate near the apex) (Fig. 1C), and the hairs on the young parts and distal portions of branchlets usually c. 0.5 mm long and appressed to spreading (vs c. 1 mm long and mostly ± spreading) (Fig. 1E). When compared with other species, this variety is most like Z. kunstleri and Z. puberula in having hairy, ellipsoid fruits > 2 cm long but differs from both in the subsessile fascicle-like cymes and fruits. Vegetatively, it differs from Z. kunstleri in the transverse veins that join the main veins usually unbranched and closely spaced, by c. 1 mm from each other and the higher order reticulations between the transverse scalariform veins that join the main veins are barely visible (vs transverse veins usually branched, spaced by c. 5 mm and with conspicuous, raised longitudinal venules between them) (Fig. 1D). It differs from Z. puberula in the conspicuous indumentum of dense hairs > 0.5 mm long on branchlets, leaves and flowers (vs minute, scarcely visible to the naked eye in Z. puberula). It differs from both Z. kunstleri and Z. puberula in the c. 8 strong marginal veins on either side rarely forming clear loops with each other but all reaching a usually well-defined intramarginal vein running along the leaf margin (vs > 10 strong marginal veins on either side in Z. puberula and > 20 in Z. kunstleri, consistently forming clear loops with each other and not joining a well-defined intramarginal vein ( Fig. 1A & B). The strong marginal veins in Z. borneensis var. borneensis are reminiscent of Z. horsfieldii but the axillary flowers, reddish indumentum and large ellipsoid fruit clearly distinguish the species. Ziziphus cumingiana var. cumingiana also has axillary, fascicle-like cymes but differs in the leaves being thin-chartaceous, with crenate margins, higher order reticulations and well-developed areoles, clearly visible with a hand lens, drying dark red and contrasting strongly with the lamina colour, and the fruits being smaller, c. 7 × 6 mm, obovoid and glabrous.

Key to varieties of
Elmer 20149, indicated as the type in the protologue (Merrill 1929), is widely distributed with duplicates available in at least 12 herbaria. The specimen from UC, where Merrill worked from 1924 -1929, and which is in flower, is selected here as the lectotype. Branchlets densely hairy on young parts and distal portions, hairs c. 1 mm long and mostly ± spreading. Leaves narrow ovate (-elliptic), (4.2 -) 5.5 (-7.5) × (1.8 -) 2.4 (-3.1) cm; callosities protruding off a margin that is finely serrate in outline, serrations clearly visible all along leaf margin; strong marginal veins coming off the outside of the two outer main veins c. 8 on either side, intramarginal vein running along the leaf margin indistinct; venation not clearly reticulate, transverse veins that join the main veins much stronger than the longitudinal venules between them; lamina subglabrous abaxially except along larger veins, marginal veins and transverse veins between the main veins. Fig. 1F -K. A sheet of Clemens & Clemens 30376 from M is marked as the holotype, and while this collection is cited in the protologue (Suessenguth 1950), additional material is available at M and other herbaria. The sheet marked as the holotype is therefore designated here as the lectotype because no specific sheet was indicated in the protologue.
Two sheets of Clemens & Clemens 30376 are also available at K, but this is a mixed collection: only Sheet 2 (marked "Sheet II") is of this variety of Ziziphus borneensis. Sheet 1 [K000723017] is a specimen of Z. havilandii.  Branchlets densely hairy on young parts and distal portions, hairs variable, usually c. 0.5 mm long, spreading to appressed. Leaves narrow ovate (elliptic-oblong), (7.2 -) 10.6 (-15.0) × (3.0 -) 4.3 (-5.3) cm; callosities protruding off a margin that is finely serrate in outline, serrations visible all along leaf margin but especially clearly near apex; strong marginal veins coming off the outside of the two outer main veins > 15 on either side, intramarginal vein running along the leaf margin very distinct; venation reticulate abaxially, with the longitudinal venules between the transverse veins that join the main veins conspicuous and raised; lamina densely hairy abaxially on its entire surface. NOTES. The leaf venation in this variety is strikingly different from other Ziziphus borneensis varieties, with > 15 strong marginal veins on either side (Fig. 1R) and the reticulations of finer venules clearly visible (Fig. 1S). It is like Z. puberula in the marginal veins > 15 (although sometimes < 15 in Z. puberula) and the big, > 2 cm, ellipsoid fruit, but differs in the dense indumentum of longer hairs on the branchlets and leaves (Fig. 1S & T), reticulation of leaf veinlets clearly visible, the presence of a distinct intramarginal vein running along the leaf margin (Fig. 1Q), subsessile fasciclelike cymes and subsessile fruit.
The variety is only known from three localities each at least 200 km apart from one another. Specimens of the Sarawak collections have a more reddish indumentum, but all share the same characteristic venation pattern. Branchlets densely hairy on young parts and distal portions, hairs c. 1 mm long and mostly ± spreading. Leaves narrow ovate, (4.6 -) 6.4 (-7.5) × (1.9 -) 2.8 (-3.5) cm; callosities protruding off a margin that is finely serrate in outline, serrations clearly visible near leaf apex only; strong marginal veins coming off the outside of the two outer main veins c. 8 on either side, intramarginal vein running along the leaf margin indistinct; venation not clearly reticulate, transverse veins that join the main veins much stronger than the longitudinal venules between them; lamina densely hairy abaxially on its entire surface. Fig. 1L -P.
RECOGNITION. This variety is most like Ziziphus borneensis var. kinabalui in the densely hairy branchlets with c. 1 mm long hairs that are mostly ± spreading and in the absence of a clearly visible intramarginal vein but differs in the abaxial lamina surface being entirely hairy (vs along major veins and transverse veins between the main veins only) and the leaf margin serrations clearly visible near the leaf apex only (vs clearly visible all along the leaf margin). DISTRIBUTION Madani SAN 36786 (K,L). HABITAT. Borneo montane rain forests; alt. c. 1300 m. CONSERVATION STATUS. Data Deficient (DD). The variety is only known from the Kundasang-Sosopodon area near Mount Kinabalu. It thus meets the IUCN B1a criterion for Critically Endangered, but a decline or fluctuation of the population cannot be estimated or inferred. The specimens may have been collected within the Sosopodon Forest Reserve (IUCN Category Ia) where despite some fragmentation, forests seem well preserved overall in satellite images. The variety is considered here to be Data Deficient because the data is so uncertain that both LC and CR are plausible categories. PHENOLOGY. Collected in fruit in April and July. ETYMOLOGY. The varietal epithet derives from the Italian velluto, velvet, itself derived from the Latin villus, hair, and refers to the dense indumentum of hairs on the abaxial surface of leaves making them soft to touch. VERNACULAR NAMES. Kangom sapuon (Ranau fide Tikau SAN 28913). NOTES. This variety differs from the other Ziziphus borneensis varieties in the combination of branchlets having dense, long, reddish, mostly spreading hairs, c. 1 mm long (Fig. 1P), strong marginal veins coming off outer main veins c. 8 on either side (Fig. 1L) and the abaxial lamina surface being completely covered in hairs (Fig. 1N). NOTES. Ziziphus calophylla is recognised by the leaves being long, usually > 10 cm, leathery, usually elliptic, ± symmetric, with only the three main veins conspicuous and a faint but distinct intramarginal vein running along the leaf margin. The species is morphologically similar to Z. suluensis, as noted by Merrill (1929), but differs in the abaxial leaf surface having no to few glands (vs many) and leaf shape usually elliptic and ± symmetric (vs ellipticoblong and asymmetric). Other differences include leaves that are more coriaceous, on average longer (c. 11 cm vs 8 cm) with the leaf base wide-cuneate to rounded (vs frequently subcordate), inflorescences more branching and with more flowers (flowers c. 16 per cyme vs 8) and fruit often more ellipsoid-obovoid (vs globose-obovoid).

Ziziphus calophylla
Ziziphus calophylla and Z. havilandii could represent two ends of a spectrum in leaf size and leaf gland abundance with Z. suluensis covering some of the middle range.
In the protologue for Ziziphus calophylla, Wallich (in Roxburgh 1824) cites material "discovered on the hill of Pulo Pinang [Penang Island] by Mr.
George Porter". Four sheets collected by Porter in Penang were located, and a K-W sheet is selected as lectotype here because it is in the East India Company Herbarium (EICH) and can be considered the 'top set' upon which Wallich worked, and the sheet selected [K001038440] has fruits, whereas the the second EICH specimen [K001038440] is sterile.
Ziziphus ornata Miq. is placed as a synonym here. As noted by King (1896), no apparent morphological character seems to separate it from Z. calophylla. In the protologue for Z. suluensis, Merrill (1926) noted the similarity between Z. suluensis and Z. ornata (=Z. calophylla), noting that "except in leaf size the characters of Ziziphus ornata Miq., ex descr., apply closely to the present species". In the protologue for Z. ornata Miquel (1856)  Woody climber to at least 15 m long; girth to at least 5 cm in diam., spiny. Branchlets terete, with longitudinal striations and many conspicuous, raised lenticels, densely hairy on young parts and distal portions, more sparsely hairy when mature, hairs c. 0.1 mm long, mostly appressed-antrorse, reddish, some whitish. Stipules modified into spines, forming clusters at the tip of developing shoots, single or 3 per node, 2 lateral and one below point of insertion of leaf or branchlet, often some deciduous and 1 or 2 remaining, spines recurved, c. 5 mm long, hairy. Leaves weakly discolorous, drying greenish-brown, paler abaxially, blade symmetric, elliptic (-wide elliptic), 6.5 -17. NOTES. Ziziphus crebrivenosa is recognised in being the only species with numerous blister-like raised lenticels on its long, to 3 cm, often ellipsoid fruits. It is most like Z. kunstleri in having leaves at least 10 cm long with clearly raised transverse veins that join the main veins on the abaxial surface and in having mature fruits to at least 2 cm in length. However, finer vein reticulations are not clearly raised in Z. crebrivenosa and transverse veins tend to join the main veins without branching (vs reticulations raised and transverse veins tending to branch in Z. kunstleri). In addition, branchlets of Z. crebrivenosa have raised lenticels whereas those of Z. kunstleri are superficial and tend to be concealed on the younger parts by the dense reddish indumentum.
Williams 2335 is designated as the type in the protologue for Ziziphus crebrivenosa (Robinson 1908) and a sheet of this material from NY where Robinson worked from 1903 to 1908 is selected here as the lectotype. Merrill (1922) highlighted the "ellipsoid, not globose, entirely glabrous, conspicuously lenticellate fruits" in his protologue of Ziziphus lenticellata but compared vegetative characters of this species to those of Z. horsfieldii. He did not consider Z. crebrivenosa in this publication despite listing it in his An Enumeration of Philippine Plants the following year (Merrill 1923). No morphological character seems to separate Z. lenticellata from Z. crebrivenosa and it is placed as a synonym here. Merrill (1922) mentions Castillo 644 and Agama 1018 in the protologue for Z. lenticellata and the sheet of Agama 1018 from A is selected as the lectotype because it is in flower unlike those of Castillo 644 and may have been examined by Merrill. Ziziphus species in Borneo, as is the sparse indumentum on the pedicels and flowers and the weakly and distantly crenate margin with a tooth and hairs inserted by the sinus of each crenation. Ziziphus cumingiana var. cumingiana shares many morphological characters with Z. oenopolia (L.) Mill. which, despite being widely distributed from India to Australia (GBIF 2019), has apparently not yet been recorded in Borneo. Both species have leaves obliquely ovate, < 10 cm in length, with strong marginal veins, subsessile fascicle-like cymes and fruits small, c. 1 cm in diam., glabrous, globose to obovoid. Ziziphus oenopolia differs from Z. cumingiana var. cumingiana in the transverse veins between the main veins strong and ascending, and the leaves densely hairy abaxially. The widespread, cultivated and sometimes naturalised Z. mauritiana and Z. jujuba also have subsessile fascicle-like cymes and globose fruits but the leaf apex is usually rounded or notched as opposed to attenuate. Lectotypes for both Z. mauritiana and Z. oenopolia were recently selected in a review of the nomenclature of the species of Ziziphus occurring in Australia (Kellermann 2020).

Ziziphus cumingiana
Ziziphus cumingiana var. pilosa Merr. (Merrill 1923: 522) differs from Z. cumingiana var. cumingiana in the more densely hairy leaf surface abaxially. The difference is marked and while specimens of this variety collected in the Philippines are available in herbaria, it is not known to have been found in Borneo. Vernacular names of Z. cumingiana in the Philippines are listed by Merrill (loc. cit.). Merrill (1906) did not designate a type specimen in the protologue for Ziziphus cumingiana but lists Cuming 453 as illustrative and a sheet of this material, which is in flower, is selected here as the lectotype.
Ziziphus bulusanensis is listed as a synonym of Z. cumingiana by Merrill (1923) but because there is no retrievable diagnosis or description associated with it, the name seems to have not been validly published.  2L) and leaves being hairy with a petiole 3 -7 mm long (vs subglabrous leaves and petiole c. 1 cm long) (Fig. 2B). The species characteristically dries yellowish. A point formed by the style remains at the apex of the fruits is visible in all Ziziphus species in Borneo except perhaps Z. domatiata, but is particularly conspicuous and rigid in this species ( Fig. 2A & L). Woody climber; girth to at least 3 cm in diam., spiny.

Ziziphus domatiata
Branchlets terete, with longitudinal striations and conspicuous, raised lenticels, hairs sparse, c. 0.5 mm long mixed with shorter hairs < 0.1 mm long, spreading to appressed-antrorse. Stipules modified into spines, single, slightly recurved, c. 2 mm long, subglabrous. Leaves weakly discolorous, drying greenish-brown, blade asymmetric, narrow ovate (ovate), 3.5 -5.5 × 1.7 -3.1 cm, chartaceous to subcoriaceous, apex attenuate to acuminate, base cuneate to subcordate, usually clearly oblique, margins weakly crenate-serrate, c. 60 serrations on either side, each serration topped by a protruding callosity that dries darker than the lamina, c. 0.1 mm long; primary veins 3, impressed adaxially, raised abaxially, hairs sparse to dense along primary veins on either side of lamina, hairs c. 0.3 mm long; strong marginal veins coming off the outside of the two outer main veins (2 -) 4 (-8) on either side, ascending and gradually diminishing, rarely forming conspicuous loops near margin¸no clear intramarginal vein running along the leaf margin present, angle of divergence with outer main veins c. 45°; transverse veins between the main veins weak but discernible, coming off midrib at c. 90°, barely raised (not readily felt by touch), spaced by c. 1 mm from each other, more often slightly zigzagging than straight; higher order reticulations barely discernible; lamina subglabrous; domatia present at the junction between the marginal veins and the outer main veins, pocket-like and with tufts of hairs; petiole slightly dorsiventrally flattened, c. 5 mm long, hairs dense, indumentum extending to widened base of main veins adaxially. Inflorescence of axillary pedunculate cymes, cymes loose dichasia (inferred from fruiting material) with usually peduncle and first 2 branches clearly elongate and next branches short and less distinct; peduncles c. 5 mm long; bracteoles not seen. Flower unknown. Fruit a drupe, ripening creamy-grey, c. 1.0 × 0.8 cm, subglobose to obovoid, glabrous, smooth; fruiting pedicels c. 3 mm × 1 mm; hypanthium remains saucer-shaped at base of fruit. Fig. 3.

RECOGNITION.
Most like Ziziphus horsfieldii in having pedunculate cymes, narrow ovate leaves, which are subglabrous abaxially except along larger veins and with tufts of hairs at the junction between the marginal and outer main veins. It differs in the glabrous, subglobose fruit, ripening creamy-grey, c. 1.0 × 0.8 cm (vs fruit densely covered in reddish hairs, obovoid, ripening yellowish-green, c. 1.1 × 1.1 cm). Vegetatively, it differs in the smaller leaves, 3.5 -5.5 × 1.7 -3.1 cm (vs 3.5 -10.0 × 1.2 -4.5 cm), weakly crenate-serrate margin with c. 60 serrations on either side (vs finely denticulate and c. 100 serrations on either side) and fewer strong marginal veins, c. 4 on either side but often less (vs c. 6 and rarely < 5  (Kartawinata 2008). Because it is known from a single location and its potential EOO is inferred to be declining, it meets the B1ab(iii) criteria for CR. PHENOLOGY. Collected in fruit in April. ETYMOLOGY. Named for the presence of domatia in the axils at the junction between the marginal veins and the outer main veins, pocket-like and with tufts of hairs. USES. Fruits edible (fide Ambriansyah & Arifin W702). NOTES. This species is only known from a single collection. Vegetatively it closely resembles Ziziphus horsfieldii in the leaves being subglabrous abaxially with tufts of hairs at the junction between the marginal veins and the outer main veins (Fig. 3D).
The only other known Ziziphus species of Borneo with glabrous fruits are Z. cuspidata and Z. cumingiana. It differs from Z. cuspidata in having abaxially glabrous leaves except along the main and marginal veins (vs usually hairy) (Fig. 3D) with c. 4 or less strong marginal veins on either side (vs c. 6) ( Fig. 3A & B), in the tufts of hairs at the junction between the marginal veins and the outer main veins (vs sometimes in the axils at the base of the 3 main veins only) (Fig. 3D), and the fruits c. 1.0 × 0.8 cm and muticous (vs c. 2 × 1.5 cm and style remains forming a rigid point) (Fig. 3E). Z. cumingiana has smaller fruits (c. 7 × 6 mm cm in diam.) inserted in subsessile fasciclelike cymes (vs pedunculate cymes) and leaves thinchartaceous (vs chartaceous to subcoriaceous), with a visibly reticulate venation drying darker than lamina surface (vs reticulation indistinct and veins drying paler than lamina surface).

Ziziphus havilandii
Ridl. (Ridley 1931: 495  glabrous when mature, hairs straight to curved, spreading to appressed-antrorse. Stipules paired, one becoming a recurved spine, c. 3 mm long, the other one fugaceous, persistent on some flowering branchlets, entire, wide ovate, c. 3 × 2 mm, hairs dense, spines on distal branchlets often closely spaced, by c. 1 cm. Leaves weakly discolorous, drying greenish-brown, blade asymmetric, narrow ovate to elliptic-oblong, (1.0 -) 2. 5 -5.5 (-6.5) × (0.5 -) 1.2 -2.5 (-3.5) 5 -5.5 × 1.2 -2.5 cm, (vs usually 8 × 3.5 cm), chartaceous (vs chartaceous-subcoriaceous), usually more asymmetric and widest near base (vs widest near middle), often denser indumentum on distal branchlets and usually smaller fruits, on average 0.9 × 0.8 cm (vs 1.2 -1.5 × 0.9 -1.5 cm). The difference between the two species is slight, they could represent a single species on the same morphological variability continuum. Ziziphus suluensis was originally described based on material collected in Tawi-tawi, close to Borneo and the species is not known to occur on more northern islands of the Philippines, also suggesting that Z. havilandii and Z. suluensis could be a single lineage restricted to Borneo's near vicinity (Sulawesi and southern Philippines). Schirarend (1995) used the character of the intramarginal vein to distinguish the two species (present in Z. havilandii, absent in Z. suluensis), but this could not be observed on all available specimens previously identified as Z. suluensis, including the type material. Ridley (1931) cited Beccari 2493 and Haviland 2134 in his protologue for Ziziphus havilandii, and he indicated that the latter specimen is the "type". A sheet of the Haviland 2134 collection is selected here as the lectotype.
9. Ziziphus horsfieldii Miq. (Miquel 1856: 643 Woody climber to at least 30 m long; girth to at least 10 cm in diam., spiny. Branchlets terete, with longitudinal striations and conspicuous, raised lenticels, hairs sparse, c. 0.5 mm long mixed with shorter hairs 0.1 mm long, mostly appressedantrorse, reddish to whitish. Stipules modified into spines, single, recurved, c. 2.5 mm long, subglabrous. Leaves weakly discolorous, drying greenish-brown, blade asymmetric, (lanceolate -) narrow ovate (-ovate), 3.5 -10.0 × 1.2 -4.5 cm, chartaceous to subcoriaceous, apex attenuate to acuminate, base cuneate to subcordate, usually clearly oblique, margins finely denticulate, c. 100 serrations on either side, each serration topped by a protruding callosity that dries darker than the lamina, c. 0.1 mm long; primary veins 3, impressed adaxially, raised abaxially, hairs sparse along primary veins on either side of lamina, often more densely adaxially, hairs c. 0.2 mm long; strong marginal veins coming off the outside of the two outer main veins c. 6 on either side, rarely < 5, ascending and gradually diminishing, not forming conspicuous loops near margin¸no clear intramarginal vein running along the leaf margin present, angle of divergence with outer main veins c. 45°; transverse veins between the main veins weak but discernible, especially adaxially, coming off midrib at c. 90°, barely raised (not readily felt by touch), spaced by c. 1 mm from each other, more often slightly zigzagging than straight; higher order reticulations barely discernible; lamina subglabrous; domatia present in the axils at the base of the 3 main veins and at the junction between the marginal veins and the outer main veins, pocket-like and often with tufts of hairs, swelling often visible adaxially just above junction between 3 main veins; petiole slightly dorsiventrally flattened, c. 7 mm long, hairs dense, indumentum extending to widened base of main veins adaxially. Inflorescence of axillary pedunculate cymes, < ½ as long as subtending leaves, c. 12 flowers in each cyme, cymes loose dichasia with usually peduncle and first 2 branches clearly elongate and next 4 branches short but distinct; peduncles dorsiventrally flattened (5 -) 10 (-15) mm long, hairs abundant, mostly < 0.1 mm long; pedicels c. 2 mm long, straight to slightly curved; bracteoles entire, narrowly triangular, c. 1 mm long, hairy. Flower faintly scented; hypanthium densely hairy on the outer surface, hairs 0.1 mm long, appressed-antrorse, greyish; sepals triangular, c. 1.2 mm long, pale greenish when fresh, glabrous and keeled adaxially; petals clawed, c. 1 mm long, obcordate, white; stamen filaments flat, subulate, c. 0.7 mm long, anthers c. 0.3 mm long, enclosed by petals; nectary disk yellow, pentagonal, 10-pitted, glabrous, annulus surrounding ovary barely raised; style arms 2, free for c. 1 mm, glabrous; ovary partially immersed, hairs dense. Fruit a drupe, ripening yellowish-green, (0.9 -) 1.1 (-1.5) × (0.7 -) 1.1 (-1.5)  In Borneo, Ziziphus horsfieldii is most like Z. cuspidata and Z. domatiata in having pedunculate cymes, fruits < 1.5 × longer than wide, leaves usually < 7 × 3 cm with usually < 8 strong marginal veins coming off the outer main veins on either side. It differs from both species in the densely hairy fruits (vs glabrous). It also differs from Z. cuspidata in the smaller fruits, c. 1.1 × 1.1 cm (vs c. 2 × 1.5 cm), the leaf lamina being subglabrous abaxially except along larger veins (vs usually hairy), the longer petioles, c. 10 mm (vs 3 -7 mm) and the often clear presence of tufts of hairs at the junction between the outer main veins and the marginal veins. It further differs from Z. domatiata in the obovoid fruits (vs subglobose) and leaves with c. 6 strong marginal veins on either side (vs. c. 4).
The type material from Java is unusual in having almost subsessile fruits but does not appear to differ in any other morphological character from material recognised here as Ziziphus horsfieldii. A lectotype is selected here among the Horsfield material collected in Java. Two additional sheets of Z. horsfieldii from Java marked as belonging to Horsfield's herbarium are available at K (K000723024, K000723026) but whether these are isolectotypes, i.e. from the same collection event as the lectotype, is unsure.
Ziziphus palawanensis Elmer is placed as a synonym here because no apparent morphological character from the type material or protologue description seems to separate it from Z. horsfieldii. Elmer (1913) described the climber as forming "dense hanging masses over the open creek bed". Elmer 12891, indicated as the type in the protologue for Z. palawanensis (Elmer op. cit.), is widely distributed with duplicates available in at least seven herbaria. and the sheet at A, where much of Elmer's herbar-ium collections are kept, is selected here as the lectotype.
apex rounded to acuminate, base rounded to cordate, symmetric, margins entire to serrate, c. 70 serrations on either side, each serration topped by a minute protruding callosity that dries darker than the lamina, c. 0.1 mm long; primary veins 3, impressed adaxially, raised abaxially, hairs abundant along primary veins abaxially, hairs c. 0.7 mm long, ± straight, ± spreading; strong marginal veins coming off the outside of the two outer main veins > 20 on either side, ± equally strong, ascending and forming loops near the margin but no clear intramarginal vein running along the leaf margin, angle of divergence with outer main veins 40 -70°; transverse veins between the main veins conspicuous, coming off midrib at 50 -90°, raised (readily felt by touch), spaced by c. 5 mm from each other, slightly zigzagging, often branching; higher order reticulations discernible, slightly raised; lamina sparsely hairy abaxially (more densely along bigger veins), hairs c. 0.3 mm long, mostly spreading; domatia present in the axils at bigger veins with main veins, pocket-like; petiole slightly dorsiventrally flattened, (2 -) 4 (-10) mm long, hairs dense, indumentum extending to widened base of main veins adaxially. Second type of leaf smaller, at the base of cymes, fugaceous, narrowly ovate, c. 5 × 2 cm, apex acute to attenuate. Inflorescence of axillary pedunculate cymes subtended by fugaceous leaves, ultimately arranged in a panicle, < ½ as long as subtending leaves, c. 7 flowers in each cyme, cymes contracted dichasia not or only once visibly branching; peduncles 2 -10 mm long, hairs dense, reddish, spreading; bracteoles entire to deeply bifid, narrowly triangular, c. 3 mm long, hairy. Flower hypanthium densely hairy on the outer surface; sepals triangular, pale yellow, c. 2 mm long, glabrous and keeled adaxially; petals clawed, c. 2.5 mm long, obcordate; stamen filaments flat, subulate, c. 2 mm long, anthers c. 0.4 mm long, enclosed by petals; nectary disk, pentagonal, 10pitted, glabrous; style arms 2, well-developed, c. 0.8 mm long, diverging, not expanding at apex, glabrous ovary partially immersed, hairs dense. Fruit a drupe, ripening with a velvety brown tinge, ellipsoid, often with a flattened base, c. (2 -) 3 × (1.5 -) 1.8 cm, indumentum dense, hairs drying reddish-brown, hypanthium remains at base of fruit visible, saucer-like, calyx lobes often persistent and reflexed. and transverse veins tend to join the main veins without branching in Z. crebrivenosa). In addition, branchlets of Z. kunstleri have superficial lenticels concealed on younger parts by the dense reddish indumentum (vs lenticels conspicuous and raised in Z. crebrivenosa). Both species occur in Borneo, but their distribution is not known to overlap elsewhere. King (1896) specified naming the species "in memory of its first collector, H. H. Kunstler, who sent it from Province Wellesley in 1881" and lists King's Collector [Kunstler] 1607 as illustrative material in his protologue for Ziziphus kunstleri. A sheet of this material is available at K, which holds King's main sets, and is selected here as the lectotype.
Ziziphus cupularis type material does not appear to differ from Z. kunstleri. In the protologue notes for Z. cupularis, Suessenguth & Overkott (1941) indicated that both species are similar but that Z. kunstleri differs in having axillary inflorescences and a hypanthium that is not cup-shaped. In Z. kunstleri, inflorescences are indeed subtended by leaves at an early stage, but these leaves, which are distinctly smaller than more proximal leaves, soon fall and inflorescences then are paniculate as in the type material for Z. cupularis. The hypanthium appears cup-shaped on most Z. kunstleri material as it does in the type material for Z. cupularis, but this is no longer obvious in specimens with fully open flowers, such as King's Collector 1607. Suessenguth & Overkott cited Native Collector 113 in the protologue for Z. cupularis. Suessenguth worked in M and a sheet with a drawing of the flower of this collection, but no plant material, and referring to material in B, is available at M [M0211790]. Suessenguth & Overkott (op. cit.) also specified that the material they studied was provided by B. The type therefore used to be there and it is most likely that it was destroyed in the 1943 fire (Merrill 1943). The sheet at K, which includes open flowers, is selected here as the lectotype.
Surprisingly, Ziziphus kunstleri was not included in the list of Ziziphus species occurring in Sabah and Sarawak by Schirarend (1995), despite being cited by Beaman & Anderson (2004), Masamune (1942) and Ridley (1931). margin (vs c. 6, ascending and gradually diminishing, not forming conspicuous loops near margin) (Fig. 4B) and the ellipsoid and bigger fruits, c. 3 × 1.7 cm (vs obovoid fruits c. 1.1 × 1.1 cm) (Fig. 4J). Tree, small [height not measured but plant described as "small tree" on lectotype label], unarmed. Crown, bole, bark, sapwood and heartwood features unknown. Branchlets terete, with longitudinal striations and visible lenticels, densely hairy on young parts and distal portions, more sparsely hairy when mature, hairs c. 0.3 mm long, mostly spreading, curved, reddish-brown. Stipules not transformed into spines, early deciduous, narrowly triangular, c. 7 mm long, densely hairy. Leaves weakly discolorous, drying greenish-brown, blade ± symmetric, elliptic-oblong, 14 -31 × 3.5 -11 cm, chartaceous to subcoriaceous, apex attenuate to acuminate, base obtuse to rounded, ± symmetric, margins subentire, obscurely serrate, each serration topped by a minute protruding callosity that dries darker than the lamina, c. 0.1 mm long; primary veins 3, impressed adaxially, raised abaxially, hairs dense along primary veins abaxially, hairs c. 1 mm long curved to tortuous, spreading to antrorse, reddish some whitish; strong marginal veins coming off the outside of the two outer main veins 30 on either side, all ending in a distinct intramarginal vein running along the leaf margin, angle of divergence with outer main veins c. 65°; transverse veins between the main veins conspicuous, also coming off midrib at c. 65°, raised (readily felt by touch), spaced by c. 5 (-15)  NOTES. Ziziphus ridleyana is most like Z. angustifolia in being a tree without spines but differs in the dense reddish-brown indumentum, covering the branchlets and abaxial surface of leaves (vs glabrous to sparsely hairy leaves, hairy on the main veins only) and bigger flowers, the sepals being c. 4 mm long (vs c. 2 mm long). This species was originally published by Ridley as Ziziphus macrophylla (1931), but the name is an illegitimate later homonym of the fossil name Z. macrophylla (Ettingsh.) Schimp. (Schimper 1874: 224), following Art. 53.1 of the ICN (Shenzen Code) (Turland et al. 2018). The matter was addressed by Rasingam & Karthigeyan (2020) who published the new name Z. ridleyana to replace the illegitimate combination. Two sheets of the same collection by Garai are available at K (K000723013 and K000723014) but only one of them, the holotype, is mentioned in the Z. ridleyana protologue (K0007230134). The date of collection of the holotype is indicated to be August 1892 in the protologue, but its label does not specify a date. The label of the isotype (K000723013) reads 'Rec d . aug 1892', which is the date the specimen was received rather than collected. Ridley (op. cit.) surprisingly compares it to the much different Z. borneensis, which is a spiny climber rather than Z. inermis (= Z. angustifolia). Ziziphus macrophylla (= Z. ridleyana) is not cited in the Tree Flora of Sabah and Sarawak (Schirarend 1995).

Ziziphus ridleyana
13. Ziziphus suluensis Merr. (Merrill 1926: 408 Woody climber to at least 15 m long, girth not recorded, spiny. Branchlets terete, with longitudinal striations and visible lenticels, sparsely to abundantly hairy on young parts and distal portions, becoming sparsely hairy to glabrous when mature, hairs straight to curved, spreading to appressed-antrorse. Stipules paired, one becoming a recurved spine, c. 3 mm long, the other one fugaceous, persistent on some flowering branchlets, entire, wide ovate, c. 3 × 2 mm, hairs dense, spines on distal branchlets often closely spaced, by c. 1 cm. Leaves weakly discolorous, drying greenish-brown, blade asymmetric, (ovate -) elliptic-oblong, (4.5 -) 8 (-13) × (1.9 -) 3.5 (-5.2) cm, chartaceous-subcoriaceous, apex attenuate to acuminate, base wide cuneate to subcordate, usually symmetric, margins subentire to finely denticulate, > 100 serrations on either side, each serration topped by a protruding callosity that dries darker than the lamina, c. 0.1 mm long; primary veins 3, impressed adaxially, raised abaxially, hairs sparse to dense along primary veins on either side of lamina, hairs c. 0.2 mm long; strong marginal veins coming off the outside of the two outer main absent (only 3 main veins conspicuous)¸faint intramarginal vein running along the leaf margin present; transverse veins between the main veins weak but discernible, coming off midrib at c. 90°, barely raised (not readily felt by touch), tightly spaced, usually < 1 mm from each other, more often slightly zigzagging than straight; higher order reticulations and areoles well-developed, visible with a hand lens; lamina subglabrous, with many glands, mostly visible abaxially, drying darker than rest of lamina surface, slightly pitted, ± 0.1 mm in diam.; tufts of hairs present in the axils at the base of the 3 main veins; petiole slightly dorsiventrally flattened, 3 -7 mm long, hairs dense, indumentum extending to widened base of main veins adaxially.