﻿Capparis (Capparaceae) in Peninsular Malaysia, including a new species and two new varieties

﻿Abstract As part of the Flora of Peninsular Malaysia Project, a species checklist of the genus Capparis in Peninsular Malaysia is presented here with a total of 11 species, two subspecies and four varieties. A new species and two varieties, endemic to Peninsular Malaysia, are described and illustrated: Cappariskenaboiensis, C.scortechiniivar.ruthiae and C.trinerviavar.chungiana. Cappariskenaboiensis is known from a single site in Negeri Sembilan and is assessed as Vulnerable (VU); C.scortechiniivar.ruthiae from Pahang is Vulnerable (VU); and Capparistrinerviavar.chungiana is known from Negeri Sembilan, Pahang and Selangor and its conservation status is assessed as Near Threatened (NT). A checklist and updated key to the genus in Peninsular Malaysia are provided.

Generic delimitation and relationships amongst Capparis species using morphological and molecular approaches have shown the New World and Old World species of Capparis do not form a monophyletic group (Hall 2008;Cardinal-McTeague et al. 2016;Tamboli et al. 2018). The New World taxa, traditionally identified as Capparis s.l., differ from Old World Capparis by the following traits: absence of prickles, symmetry of flowers, calyx types, calyx and corolla aestivation, different floral nectary structures and different fruit and embryo types (Cornejo and Iltis 2009a). Thus, all species of Capparis in the Neotropics belong to other genera, with the species now transferred into several genera (e.g. Cornejo and Iltis 2008, 2009a, 2009bCornejo 2017).
In Peninsular Malaysia, at least ten species and two subspecies were known Turner 1995;Kiew et al. 2009) -all members of sect. Monostichocalyx, characterised by the well-developed persistent leaves, sepals free in bud and dimorphic in which the outer sepals are larger in size, enclosing the narrower inner pair of sepals (Jacobs 1960: 410). These members were placed into four groups within this section: Capparis scortechinii King and C. trinervia Hook.f. & Thoms. in the Trinervia-Group; C. diffusa Ridl., C. erycibe Hallier f., C. sepiaria L. and C. versicolor Griff. in the Subumbellates-Group; C. pubiflora DC. in Cataphyllosa-Group; and C. acutifolia Sweet, C. cucurbitina King and C. micracantha DC. in the Seriales-Group. Of these ten species, C. cucurbitina was the only endemic to Peninsular Malaysia, being known from Gunung Bubu, Perak.
During a study of Capparis specimens for revisionary work on the genus for the Flora of Peninsular Malaysia account, several specimens which were determined as previously-described species (following Jacobs 1965) were critically re-evaluated as two undescribed taxa. These two are clearly distinct in several of their vegetative and reproductive characters from any known species. Another taxon discovered during the 2014 expedition to Kenaboi Forest Reserve (FR), Negeri Sembilan, also represents an undescribed taxon. After morphological comparison with closely related species (see below) and consulting the relevant literature Chayamarit 1991;Srisanga and Chayamarit 2004;Zhang and Tucker 2008;Fici 2012Fici , 2016Fici , 2021Thuong et al. 2013Thuong et al. , 2015Thuong et al. , 2016Thuong et al. , 2017Fici et al. 2018;Souvannakhoummane et al. 2018;Souvannakhoummane et al. 2020), these taxa are here recognised as three new taxa. Subsequently, in the checklist presented here, there are 11 species of Capparis in Peninsular Malaysia, with two subspecies and four varieties; all taxa are members of sect. Monostichocalyx. In addition to these three new taxa, Peninsular Malaysia now has four endemic taxa of Capparis. A key is provided to facilitate identification of the species.

Materials and methods
Morphological observations were made from herbarium material held at BKF, K, KEP, KLU, L, SAN and SING. Specimens deposited in CAL were studied, based on scanned images. Additionally, specimen images from Global Plants JSTOR (http://plants.jstor. org/), Conservatoire & Jardin botaniques de la Ville de Genève. (http://www.ville-ge. ch/musinfo/bd/cjb/chg) and the BioPortal of Naturalis Biodiversity Center (http:// bioportal.naturalis.nl/) were consulted. Floral measurements were made from either rehydrated or fresh material; details are given, based on specimen labels. Flowering and fruiting materials are indicated by 'fl.' and 'fr.', respectively, under the specimens examined section for the new taxa. Specimens were mapped and a conservation assessment of the species undertaken using the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012 following the guidelines and procedures developed at FRIM for the Malaysia Plant Red List (Chua and Saw 2006).

Taxonomic treatment
Capparis L.
Shrubs, often sprawling or climbing, rarely small trees. Twigs flexuous or straight. Indumentum mostly simple hairs, sometimes stellate, often glabrescent. Stipular thorns and/or prickles straight or retrorse, divaricate, often well-developed and persistent on main branches, sometimes rudimentary (rarely lacking). Leaves alternate or spirally arranged; lamina simple, coriaceous, subcoriaceous or chartaceous, sometimes extra membranous, margin entire, edges flat or recurved, lateral veins ascending regularly, sometimes brochidodromous interlooping near the margin. Inflorescence axillary, lateral or terminal; bracts mostly present, but early caducous, rarely to basal bracteoles. Flowers solitary or fascicle in the axils or in a series with 2-6-flowered along the twig or arranged in corymbs, umbels or subumbels or paniculate; sepals free in bud, 4, arranged in pairs and opposing sepals equal in size, imbricate or not; petals 4, asymmetrical, the dorsal petals erect and laterally connate at base, lateral ones spreading and free, rather delicate; stamens 6 to numerous, filaments of unequal length, anthers tetrasporangiate, basifixed or dorsifixed, opening lengthwise; ovary 1-locular, on gynophores as long as the stamens or longer, not or very little stretching in fruit, stigma obscure or small, sessile (elsewhere and in Peninsular Malaysia) or in capitate or cushion-shaped (elsewhere, but not in Peninsular Malaysia). Fruit an amphisarca with a subwoody (when young) turning pulpy (when ripe) exocarp, indehiscent (elsewhere and in Peninsular Malaysia) with the exception of Capparis cartilaginea Decne. and C. spinosa L. (a capsular: ripened fruit dehiscent longitudinally), globose, ellipsoid or torulose, exocarp smooth with or without longitudinal ribs (fruit is without longitudinal ribs in Peninsular Malaysia) or tuberculate (elsewhere, but not in Peninsular Malaysia). Seeds few to many rarely 1; embryo tightly coiled with the cotyledons in the centre; cotyledons stipulate, ovate or elliptic, white.

Groups of sect. Monostichocalyx
Capparis sect. Monostichocalyx, distributed from Africa (except the northern part) to Asia, extended to Australia and the Pacific, contains the majority of species in the genus with ca. 110 taxa Srisanga and Chayamarit 2004;Fici 2012Fici , 2021Thuong et al. 2013Thuong et al. , 2015Thuong et al. , 2016Thuong et al. , 2017Fici et al. 2018;Souvannakhoummane et al. 2018). Members of this section have been divided into seven groups, but Peninsular Malaysian taxa fall into four groups as mentioned earlier in introduction.
Ecology. Secondary forest margin, in light shade.

Conservation status.
Capparis kenaboiensis is known from a single locality and is very rare with less than ten individuals found in two subpopulations. The species inhabits a secondary forest margin and by a pathway, which are vulnerable to forest clearing pathways as was observed in 2014 during the botanical survey. Moreover, only two sub-populations were observed during a recent visit in 2019. As the area of occupancy is less than 500 km 2 and the declining of habitat, this species is assessed as Vulnerable B2ab(iii), following the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012. Notes. Capparis kenaboiensis (Figs 2, 3) is characterised by the flowers, loosely arranged in the raceme with each single flower subtended by a leaf-like bract. Vegetatively, Capparis kenaboiensis resembles C. buwaldae from the Seriales-group, but its short racemose inflorescences subtended by leaves are similar to members of the Subumbellates-Group. Characterised further by the small size of flowers with sepals 6-8 mm long and the plants hairy on young parts, Capparis kenaboiensis is best placed within the Subumbellates-Group (Jacobs 1965: 412). Further morphological comparison of this new species with other closely related species is as indicated in the Table 1.
Ecology. On degraded hill slopes and open areas along the forest margins, gaps or roadsides, hill forest to lower montane forest at ca. 1280 m elevation.
Etymology. This new variety is named after Dr Ruth Kiew, collector of type specimen and the Flora of Peninsular Malaysia project co-ordinator and consultant.
Conservation status. Capparis scortechinii var. ruthiae was conspicuous and inhabits forest margins, gaps or pathway near roadsides, but has not been relocated after 1993 at the original localities and adjacent areas even though they have been revisited many times. As the estimated extent of occurrence is less than 500 km 2 and the declining of habitat quality, this variety is assessed as a Vulnerable B2ab(iii), following the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012.

Notes.
Amongst the known members of Trinervia-group, Capparis scortechinii var. ruthiae (Fig. 5) is closely related to var. scortechinii because both are characterised by the compact racemes. However, the new species has racemes strictly in terminal (but axillary rarely terminal in var. scortechinii) and the leaf-like bracts are smaller and greenish with tomentose, straw hairs on both surfaces, which is glabrescent with age abaxially (compared to a larger and prominent of velvety, shiny, rusty hairs in var. scortechinii).
The new variety also differs in its entirely glabrous filament and gynophore (while var. scortechinii has the filament and gynophore densely hairy at the base), the petals are loosely ciliate along the margin (but glabrous in var. scortechinii), and the inner pair of sepals are glabrous along the margin (but ciliate in var. scortechinii).
Flowers with a vestigial and well-developed gynoecium are presented in Capparis scortechinii var. scortechinii, but only well-developed gynoecium observed in var. Diagnosis. Recognised in the genus Capparis by the combination of the following characters: the leaves broadly ovate-elliptic, relatively large (13-16 × 5.5-8.5 cm) and leaves drying reddish-brown, rarely pale green with pale yellow and rarely dark red venation, the tertiary venation obscure, the inflorescence strictly terminal with flowers arranged racemosely and becoming crowded at the distal part of the inflorescence, the stamens 30-40 and the fruit globose with ca. 11 cm in diameter.
Etymology. The new variety is named after Dr Richard Chung Cheng Kong, Curator of the Kepong Herbarium (KEP) and Project Leader of Flora of Malaysia under 10 th and 11 th Malaysian Plans.
Conservation status. Capparis trinervia var. chungiana inhabits forest margins, gaps or pathways near to roadsides, but is not a common species. This species has not been relocated in Selangor and Pahang even though the localities and adjacent areas have been revisited. This species, however, has been found and recorded from a new locality in Negeri Sembilan during a botanical survey in 2010, but it could not be relocated from two recent visits in 2014 and 2019. Recent field observations to Negeri Sembilan also show forest clearing pathways near the species habitat. Therefore, this species is assessed as Near Threatened following the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012. Notes. The comparatively large flowers, with sepals up to 1.5 cm long, place Capparis trinervia var. chungiana (Figs 7,8) in the Trinervia-Group Srisanga and Chayamarit 2004). Specimens of this new species were determined as C. erycibe, no doubt due to the comparatively large leaves, but it differs in having the flowers arranged racemosely and becoming crowded at the distal part of the inflorescence rather than the paniculate arrangement in C. erycibe. In addition, C. erycibe has smaller flowers with sepals only 4-6 mm long and was placed within the Subumbellates-group (Jacobs 1965: 411).
The flower colour of this species has been described as 'white' or 'cream' with pink or dark purple at base in the label notes. Unfortunately, the open flowers are missing from the specimen sheets. Additionally, there are no new flowering specimens from the recent collections and full details of the flowers, such as measurement of the mature flowers and bracts, remain incomplete. Moreover, the dissected parts of the rehydrated flower buds are in poor condition and mostly do not contain either androecium or gynoecium, the cause of which is unknown.
However, this new variety still can be distinguished from other closely related members of the Trinervia-Group (see Table 2 for the comparison details) or species known from Peninsular Malaysia vegetatively. For example, the relatively large fruit (ca. 11 cm in diam.) of Capparis trinervia var. chungiana is similar to C. scortechinii (ca. 11 cm in diam.) and C. trisonthiae from Thailand (6-8 cm in diam.), but the latter two differ in their densely racemose and paniculate inflorescences, respectively; and the flowers arranged racemosely and becoming crowded at the distal part of the inflorescence, though has similarity to typical var. trinervia, but var. chungiana differs by its subcoriaceous to coriaceous leaves with broadly ovate to ovate-elliptic lamina (compared to chartaceous with oblong-elliptic or broadly lanceolate lamina in var. trinervia), the drying leaves are reddish-brown, rarely pale green with venation pale yellow, rarely dark red on both surfaces (compared to dull green with brownish main nerves on both surfaces in var. trinervia), the intercostal veins are obscure (compared to irregular reticulate and distinct in var. trinervia) and the stamens are 30-40 (whereas in var. trinervia, (30-)60-70).

Capparis diffusa
Conservation status. There are several voucher specimens which have been collected as recently as 2008. None of the habitats is within protected areas. As the estimated extent of occurrence is less than 20,000 km 2 and the quality of habitat is declining, Capparis diffusa is assessed as Vulnerable B1ab(iii), according to the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012. Notes. Amongst the species with small leaves, Capparis diffusa is distinguished by its terminal or lateral inflorescences on short twigs and the 3-5-flowered in umbellate arrangement, with 1-2 small leaves, sometimes a few umbels united to a small panicle and sessile.

5.
Capparis erycibe Hallier f. Bull. Herb. Bossier 6 (1898) 216; Jacobs, Fl. Malesiana 1, 6 (1960) 75, fig. 8, Blumea 12, 3 (1965) 449; Chayamarit, Fl. Thailand 5, 3 (1991)  Conservation status. This species is very rare since it has been collected only twice, the last time being in 1917. Although a fieldwork expedition has been made to the localities, Capparis erycibe could not be located. As the estimated of extent occurrence is less than 100 km 2 and the declining of habitat quality, in which the type locality was converted into an oil palm estate, the species could be assessed as Critically Endangered, according to the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012. However, the species has also been collected from a National Park, which is a protected area. Therefore, this species is assessed as Near Threatened. Ecology. In the lowland tropical forests. Distribution. Capparis micracantha subsp. korthalsiana is distributed in the southern part of Peninsular Malaysia and it has been collected from Pahang (Rompin) and Johor (Mersing and Masai).
Conservation status. Capparis micracantha subsp. korthalsiana has been found and collected only four times, the last time being in 1967. With small distribution, the extent of occurrence less than 5000 km 2 and the declining of habitat, C. micracantha subsp. korthalsiana could be assessed as Endangered, according to the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012. However, C. micracantha subsp. korthalsiana was also found from Pulau Aur, which is a protected habitat under the Marine Park Act. Thus, C. micracantha subsp. korthalsiana is assessed as Near threatened. Ecology. Its habitat preference is for wetter forest than that preferred by C. micracantha subsp. Notes. Capparis micracantha subsp. korthalsiana differs from C. micracantha subsp. micracantha in several aspects, but easily distinguished by its inflorescences being supraaxillary, either solitary or in pairs and the stamens are numerous. 8. Capparis pubiflora DC. Prod. 1 (1824) 246; Jacobs, Fl. Malesiana 1, 6 (1960) 82, figs 16, 17, Blumea 12 (1965Chayamarit, Fl. Thailand 5, 3 (1991) 258.
Conservation status. Capparis pubiflora is found and collected mostly from limestone hills with a recent collection from Gua Musang (FRI94559). None of the localities is within protected areas and some limestone hills are active quarries. Therefore, this species is assessed as Near Threatened.
Distribution. In Peninsular Malaysia so far collected from Kedah (Alor Setar) and Kelantan. Recent surveys in 2010 were unable to locate the species.
Conservation status. Data Deficient. Ecology. Found in hill forest at low altitude, 122-244 m.
Notes. This species is best distinguished from others by combination of several characters: the leaves are trinerved at base and the irregular reticulate venation distinct on both surfaces and the inflorescences are terminal with flowers arranged in subumbels. Distribution. In Peninsular Malaysia, recorded so far from Perak (Larut and Kampar). Conservation status. This species is very rare with only two specimens recorded from Perak and it was last collected in 1898. As the estimated extent of occurrence is less than 5000 km 2 and the declining of habitat quality, Capparis versicolor is assessed as Endangered B1ab(iii), according to the IUCN Red List Categories and Criteria (IUCN 2001(IUCN , 2012.
Notes. Capparis versicolor is amongst the species having relatively small leaves less than 5 cm long. It has a simple corymb inflorescence terminally on a short lateral twig with few leaves below.