A checklist of Euphorbiaceae in Bhutan with a new record of the genus Sumbaviopsis

Article information

Korean J. Pl. Taxon. 2024;54(4):304-310
Publication date (electronic) : 2024 December 31
doi : https://doi.org/10.11110/kjpt.2024.54.4.304
Ugyen Wangchuck Institute for Forestry Research and Training, Lamai Goenpa, Chhokhor, Bumthang 34005, Bhutan
Corresponding author Jigme WANGCHUK E-mail: jickmew@gmail.com
Received 2024 September 8; Revised 2024 December 12; Accepted 2024 December 25.

Abstract

The Euphorbiaceae, known for their significant diversity, are particularly abundant in tropical regions and have undergone several taxonomic reclassifications. Bhutan’s lowland tropical forests remain the least explored in this family, creating a gap in the floral database. The genus Sumbaviopsis J. J. Sm., unrecorded in Bhutan, was encountered during a field visit. We report Sumbaviopsis albicans (Blume) J. J. Sm. as a new species record for Bhutan. Following recent taxonomic revisions and current newfound species, Bhutan now lists 41 species and 17 genera within Euphorbiaceae. This newly found species contributes to the country’s floristic database, enhancing the understanding of the biodiversity of the country.

INTRODUCTION

Globally, Euphorbiaceae Juss. comprises about 330 genera and 6,300 species, with new genera continuously being added through taxonomic revisions substantiated by molecular phylogenetic studies (Cheek et al., 2016) and recently discovered novelties (Athiê-Souza et al., 2015; Zhou et al., 2017). Generally, members of the Euphorbiaceae are found in tropical climates characterized by warm, humid environments. However, some species grow in subtropical and temperate regions with mild winters and hot summers. The highest diversity is observed in the tropical areas of Africa, and the Americas, with notable hotspots in Madagascar, Central and South America, and Southeast Asia.

In Bhutan, the Euphorbiaceae was reported to comprise 29 genera and 82 species, according to the works of Grierson and Long (1987). These include Euphorbia L. (12); Pedilanthus Poiteau (1), Bridelia Willd. (5), Phyllanthus L. (11), Flueggea Willd. (1), Glochidion J.R.Forst. & G.Forst. (8), Breynia J.R.Forst. & G.Forst. (1), Sauropus Blume (3), Drypetes Vahl (2), Aporosa Blume (1), Antidesma L. (3), Baccaurea Lour. (1), Jatropha L. (2), Croton L. (5), Codiaeum Jussieu (1), Manihot Millier (1), Ostodes Blume (1), Claoxylon Jussieu (1), Mercurialis L. (1), Acalypha L. (3), Alchornea Swartz (2), Trewia L. (1), Mallotus Loureiro (4), Cleidion Blume (1), Macaranga Petit-Thouars (2), Homonoia Loureiro (1), Ricinus L. (1), Baliospermum Blume (3), and Sapium Browne (3). However, due to taxonomic revisions, many species names have been synonymized, and several names have been reclassified based on molecular phylogenetic studies (Wurdack et al., 2004, 2005; Hoffmann et al., 2006; Tokuoka, 2007). The heterogeneity, circumscription, classification, and affinities of the Euphorbiaceae have long been controversial (Tokuoka, 2007), and an attempt to dismember the family and species has been proposed (Webster, 1987). For example, the genus Antidesma L., Aporosa Blume, Baccaurea Lour., Bridelia Willd., Breynia J. R. Forst. & G. Forst., Flueggea Willd., Glochidion J. R. Forst. & G. Forst. Phyllanthus L. historically placed under Euphorbiaceae, has been reclassified to the Phyllanthaceae. At the same time, Drypetes Vahl is moved to Putranjivaceae due to plastid rbcl DNA analysis (Wurdack et al., 2004), which are listed (Table 1). This reclassification includes 32 and 2 species from Phyllanthaceae and Putranjivaceae respectively, which were reported by Grierson and Long (1987) within the Euphorbiaceae. Considering these taxonomic advancements, Bhutan has 17 genera, and 40 species under the Euphorbiaceae, with accepted names ascertained through the online databases such as World Flora Online (WFO), Plants of the World Online, and the Global Biodiversity Information Facility. Acalypha spiciflora Burm.f. (synonym: Cleidion spiciflorum (Burm.f.) Merr.) is currently unresolved name in Plants of the World Online and has been excluded from the species list (Table 1).

Accepted names of Euphorbiaceae species in Bhutan and their synonyms in the Flora of Bhutan, with circumscription to Phyllanthaceae and Putranjivaceae, reflecting recent taxonomic revisions.

The classification within the Euphorbiaceae has undergone significant revisions, as illustrated by the reclassification of Sumbaviopsis J. J. Sm. This monotypic genus was described by Johannes Jacobus Smith in 1910, a Dutch botanist, based on specimens from the Indonesian archipelago. The genus Sumbaviopsis is derived from the genus Sumbavia Baill., which was named after the island of Sumbawa in Indonesia. The suffix “-opsis” means “resembling,” reflecting its similarity to Sumbavia. Initially, species were described under the genus Sumbavia: S. rottleroides Baill. in 1858 and later S. macrophylla Müll. Arg. in 1864 (Shaw, 1960). After its initial description, Sumbaviopsis albicans was classified under several different genera, including Rottlera, Croton, and Cephalocroton, before Smith established it under Sumbaviopsis. Additionally, Müller-Argoviensis independently described it as Coelodiscus speciosus Müll.Arg. in 1865 (Muller, 1866). However, S. rottleroides was later found to be antedated by Doryxylon Zoll., with the correct name being Doryxylon spinosum Zoll., restricted distribution in Philippines, Java, Bima, and Sumbawa. Doryxylon and Sumbaviopsis can be subsumed into one genus by Balakrishnan (1967). Further, a close examination of preserved material at Kew determined that S. macrophylla is the same species as S. albicans, which was first described by Blume in 1825 and provisionally placed in the genus Adisca Blume (Shaw, 1960; Welzen, 1999). The study of Sumbaviopsis is complicated by the rarity of mature flowers in collected specimens, leading to an incomplete understanding of its unique reproductive structures and variability in features such as the torus, leaf shape, and fruit morphology (Welzen, 1999). The species Sumbaviopsis albicans has not been recorded in Bhutan, despite similar climatic conditions existing in the southern belt of the country. This highlights a gap in Bhutan’s botanical records. This research aims to establish a database for Sumbaviopsis albicans in Bhutan, addressing this gap and contributing to the understanding of this species. By documenting this species for the first time in Bhutan, the study will update the floristic records and provide insights into the distribution and ecological significance of Sumbaviopsis.

MATERIALS AND METHODS

During a field visit to the subtropical belts of Bhutan by the Nature Guide and Professional Forester, the species was observed along the feeder road connecting Panbang and Mothanguri in the Zhemgang District. Specimens were collected, and photographs of different plant parts were taken to examine morphometric traits. The herbarium specimens were collected and maintained as per the guidelines of Jain and Rao (1977), Woodland (1997), and Thiers (2017). Photographic images and herbarium specimens were later examined using a digital floral database including World Flora Online, Plants of the World Online, and the Global Biodiversity Information Facility. The species morphometric characters were validated using related articles by various authors (Welzen, 1999; Wurdack, 2004; Kathriarachchi et al., 2005; Huaxing and Gilbert, 2008) and compared with regional floral databases such as the eFloras of India, China, and Thailand. This analysis confirmed that the species is Sumbaviopsis albicans, which had not previously been recorded in the flora of Bhutan.

TAXONOMIC TREATMENT

Key to the genus Sumbaviopsis, distinguishing it from similar genera Mallotus, Doryxylon and Melanolepis

  • 1. Plants with stellate hairs or scales; inflorescences terminal or axillary panicles; fruit a capsule, often covered with hairs or glands ······························································· Mallotus

  • 1. Plants glabrous or with simple pubescence; inflorescences racemose, fasciculate, or clustered; fruit dry and dehiscent.

    • 2. Inflorescences racemose or clustered; seeds prominently carunculate ···················································· Doryxylon

    • 2. Inflorescences fasciculate or solitary; seeds not prominently carunculate.

      • 3. Plants evergreen trees or shrubs; leaves membranous, margin entire, without glands; inflorescences fasciculate; fruit dry with dehiscent capsule ······························· ······························································ Sumbaviopsis

      • 3. Plants shrubs or small trees; leaves chartaceous to subcoriaceous, often with glandular structures; inflorescences racemose, sometimes fasciculate; fruit a schizocarp, splitting into multiple segments ········ ································································ Melanolepis

Sumbaviopsis J. J. Sm. Meded. Dept. Landb. Ned.-Indië 10: 356, 1910.

Plants typically trees or large shrubs. Leaves simple, alternate, peltate, and often have entire margins; petiolate with small deciduous stipules; blades pinnately veined, with well-developed secondary veins. Flower monecious, small and inconspicuous, lacking petals, and usually borne in terminal inflorescences; pedicels with distinct longitudinal grooves. Male flowers distal, with many stamens; calyx 5-lobed, valvate; petals 5 or 10; filaments free; anthers 2-locular; receptacle convex and pubescent. Female flowers 1 to a few at the base, apetalous; calyx 5-lobed with imbricate lobes; disk annular; style recurved, 2-lobed; ovary 3-locular; ovule 1 per locule. Fruits capsules, 2-3-locular, dehisce to release seeds; each capsule contains several small seeds, typically with a fleshy aril. Torus, petioles, inflorescences, and pedicels exhibit distinct longitudinal grooves.

Sumbaviopsis albicans (Blume) J. J. Sm., Meded. Dept. Landb. Ned.-Indië 10: 357, 1910 (Fig. 1).—TYPE: Without collector’s name and number (holotype: L, barcode L0023770) Java Prov. Tjanjor.

Fig. 1.

Sumbaviopsis albicans (Blume) J. J. Sm. A. Habit with adaxial leaves. B. Abaxial leaf. C. Inflorescence with young fruits.

Adisca albicans Blume, Bijdr. Fl. Ned. Ind. 611, 1826; Doryxylon albicans(Blume) N. P. Balakr., Bull. Bot. Surv. India 9:58, 1968.

Sumbavia macrophylla Müll.Arg., Flora 47: 482, 1864.

Sumbaviopsis albicans var. disperma Gagnep., Fl. Indo- Chine 5: 420, 1925.

Shrubs to trees, up to 5–10 m tall, branchlets white or ochraceous tomentulose when young; outer bark light brown to blackish green molted with whitish green, smooth to scaly. Leaves: stipules 0.4–0.6 mm; petiole 3–8 cm long; leaf blade ovate-oblong to oblong, 10–30 × 5–15 cm, thickly papery, narrowly peltate by 2–8 mm, abaxial surface greyish-white or ochraceous tomentulose, adaxial surface dark-green, glabrous, base obtuse, apex acuminate or acute, venation impressed above raised below with 10–12 per side. Inflorescences brown-whitish; pedicels white; buds brown, staminate ones up to 16 cm long, pistillate up to 38 cm long. Bracts subovate, 2.5–3 mm. Staminate flowers 8–11 mm in diam.; pedicles ca. 2.2–4 mm long; calyx 5-lobed, ca. 5 mm, stellate-tomentose, 2.5–3 mm; disk absent; sepals 4.2–5.8 × 2–3.2 mm, brown; petals ovate 1.7–2.8 × 1.7–2.5 mm, pale green; stamens 50– 70; filaments 2.5–2.8 mm long, white; anthers 1–1.1 × 0.6– 0.6 mm, white to yellow, torus up to 1.4 mm high. Pistillate flowers ca. 3.3 mm diam.; pedicel 2.8–3.5 (–4.2 in fruit) mm long; calyx lobes ovate-oblong or lanceolate 2.3–4 × 1.5–2.5 mm; ovary stellate-tomentose, 2.7–4.5 × 2.7–3.5 mm wide; style 3, 2–3 mm long, stigmas spreading, up to 3 mm long with up to 1 mm split. Capsules 2.1–3.6 × 1.4–3 cm, globose with visible internal locules, ochraceous tomentose, processing white latex; pedicels ca. 1 cm. Seeds subglobose 12–20 × 12– 15 mm, marbled, black, hilum 1.2–2.22 × 2–4 mm; cotyledons white.

Flowering: April–June.

Fruiting: June–September.

Specimen examined: BHUTAN. Zhemgang District, Ngangla, Panbang, Ngagpati along the road connecting Panbang and Manas (Mothanguri), ca. 3 kilometers aerial distance downstream of main Panbang town, 26.826431N, 90.942209E, elev. 143 m, 21 May 2024, Tshering TT0015 (UWIFoRT), and Ngangcho, right bank of Manas river, or opposite valley of Royal Manas National Park Range Office, before 1.7 km reaching to the Bhutan-India boarder 26.801599N, 90.960981E, elev. 68 m, 22 May 2024, specimen not collected.

Distribution: Bhutan, Bangladesh, Borneo, China South- Central, India (Assam, Nagaland, and Tripura), Java, Laos, Malaysia, Myanmar, Philippines, Sulawesi, Sumatera, Thailand, Vietnam.

Taxonomic notes: The closest species to Sumbaviopsis albicans is Melanolepis multiglandulosa (Reinw. ex Blume) Rchb. & Zoll., but they can be distinguished by leaf and fruit characteristics. Sumbaviopsis albicans has membranous leaves with an obtuse base, narrowly peltate shape, ovate-oblong to oblong blade, and white abaxial surface, with a glabrous adaxial surface. In contrast, M. multiglandulosa has chartaceous leaves that are typically acutely 3-lobed, with a cordate to truncate base, ovate-orbicular or ovate-triangular shape, and a repanddentate margin. The fruit of S. albicans are capsules 2.5–3 cm in diameter with large, marbled seeds, while M. multiglandulosa has 2-lobed fruits 8–10 mm wide with smaller seeds and a purplish aril.

Ecology: Sumbaviopsis thrives in primary and secondary lowland tropical forests and often grows in areas with well-drained soils and high annual rainfall. The locality where this species occurs has substrates primarily composed of limestone, in hilly areas mixed with dipterocarps forest. The associated soils are rich, loamy, and sandy, found at elevations between 100 and 800 meters above sea level. It was also observed this species grows in both full sun and partial shade. The fruits are edible and likely contribute to the biodiversity of lowland forests by providing habitat and food for mammals, insects, and birds. Specific uses of this species are not documented, it may be locally used for construction and the tree could have medicinal or cultural significance.

Acknowledgements

The authors would like to extend deep gratitude to the management of the Ugyen Wangchuck Institute for Forestry Research and Training and the Department of Forests and Park Services for their continued guidance and support of this work.

Notes

CONFLICTS OF INTEREST

The authors declare that there are no conflicts of interest.

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Article information Continued

Fig. 1.

Sumbaviopsis albicans (Blume) J. J. Sm. A. Habit with adaxial leaves. B. Abaxial leaf. C. Inflorescence with young fruits.

Table 1.

Accepted names of Euphorbiaceae species in Bhutan and their synonyms in the Flora of Bhutan, with circumscription to Phyllanthaceae and Putranjivaceae, reflecting recent taxonomic revisions.

Sl. No. Accepted name Synoymized species of Grierson and Long, 1987 References
Euphorbiaceae
1 Acalypha brachystachya Hornem. - Grierson and Long (1987)
2 Acalypha hispida Burm. f. - Grierson and Long (1987)
3 Acalypha wilkesiana Müll. Arg. - Grierson and Long (1987)
4 Alchornea mollis (Benth.) Müll. Arg. - Grierson and Long (1987)
5 Alchornea tiliifolia (Benth.) Müll. Arg. - Grierson and Long (1987)
6 Balakata baccata (Roxb.) Esser Sapium baccatum Roxb. WFO (2024)
7 Baliospermum calycinum var. calycinum Baliospermum corymbiferum Hook.f. WFO (2024)
8 Baliospermum calycinum var. densiflorum (D.G.Long) Chakrab. & N.P.Balakr. Baliospermum densiflorum D. G. Long WFO (2024)
9 Baliospermum calycinum var. nepalense(Hurus. & Yu. Tanaka) Chakrab. & N. P. Balakr. Baliospermum nepalense Hurus. & Yu. Tanaka WFO (2024)
10 Codiaeum variegatum (L.) Rumph. ex A. Juss. - Grierson and Long (1987)
11 Croton bonplandianus Baill. - Grierson and Long (1987)
12 Croton caudatus Geiseler - Grierson and Long (1987)
13 Croton joufra Roxb. - Grierson and Long (1987)
14 Croton persimilis Müll. Arg. Croton roxburghii N. P. Balakr. WFO (2024)
15 Euphorbia griffithii Hook. f. - Grierson and Long (1987)
16 Euphorbia hirta L. - Grierson and Long (1987)
17 Euphorbia hypericifolia L. - Grierson and Long (1987)
18 Euphorbia leucocephala Lotsy - Grierson and Long (1987)
19 Euphorbia milii Des Moul. Grierson and Long (1987)
20 Euphorbia prostrata Aiton - Grierson and Long (1987)
21 Euphorbia pseudosikkimensis (Hurus. & Yu. Tanaka) Radcl.-Sm. Euphorbia longifolia D. Don. WFO (2024)
22 Euphorbia pulcherrima Willd. ex Klotzsch - Grierson and Long (1987)
23 Euphorbia royleana Boiss. - Grierson and Long (1987)
24 Euphorbia stracheyi Boiss. *Euphorbia himalayensis (Klotzsch) Boiss. WFO (2024)
25 Euphorbia thymifolia L. - Grierson and Long (1987)
26 Euphorbia tithymaloides L Pedilanthus tithymaloides (L.) Poit. WFO (2024)
27 Falconeria insignis Royle Sapium insigne (Royle) Trimen WFO (2024)
28 Homonoia riparia Lour. - Grierson and Long (1987)
29 Jatropha curcas L. - Grierson and Long (1987)
30 Jatropha podagrica Hook. - Grierson and Long (1987)
31 Macaranga denticulata (Blume) Müll. Arg. *Macaranga pustulata King ex Hook. f. WFO (2024)
32 Mallotus nepalensis Müll. Arg. - Grierson and Long (1987)
33 Mallotus nudiflorus (L.) Kulju & Welzen Trevia nudiflora L. WFO (2024)
34 Mallotus philippensis (Lam.) Müll. Arg. - Grierson and Long (1987)
35 Mallotus tetracoccus (Roxb.) Kurz - Grierson and Long (1987)
36 Manihot esculenta Crantz - Grierson and Long (1987)
37 Mercurialis leiocarpa Siebold & Zucc. - Grierson and Long (1987)
38 Ostodes paniculata Blume - Grierson and Long (1987)
39 Ricinus communis L. - Grierson and Long (1987)
40 Triadica sebifera (L.) Small Sapium sebiferum (L.) Dum. Cours. WFO 2024
Phyllanthaceae
1 Antidesma acidum Retz. - Wurdack et al. (2004)
2 Antidesma montanum var. montanum Antidesma acuminatum Wight Wurdack et al. (2004)
3 Aporosa octandra (Buch.-Ham. ex D. Don) Vickery - Wurdack et al. (2004)
4 Baccaurea ramiflora Lour. - Wurdack et al. (2004)
5 Breynia androgyna (L.) Chakrab. & N. P. Balakr. Sauropus androgynus (L.) Merr. Wurdack et al. (2004)
6 Breynia repanda (Müll. Arg.) Chakrab. & N. P. Balakr. Sauropus repandus Müll. Arg. Wurdack et al. (2004)
7 Breynia retusa (Dennst.) Alston - Wurdack et al. (2004)
8 Bridelia glauca Blume Bridelia pubescens Kurz Wurdack et al. (2004)
9 Bridelia retusa (L.) A. Juss. - Wurdack et al. (2004)
10 Bridelia sikkimensis Gehrm. - Wurdack et al. (2004)
11 Bridelia stipularis (L.) Blume - Wurdack et al. (2004)
12 Bridelia tomentosa Blume - Wurdack et al. (2004)
13 Flueggea virosa (Roxb. ex Willd.) Royle - Grierson and Long (1987)
14 Glochidion acuminatum Müll. Arg. - Wurdack et al. (2004)
15 Glochidion bourdillonii var. bhutanicum (D. G. Long) Chakrab. & M. Gangop. Glochidion bhutanicum D. G. Long Wurdack et al. (2004)
16 Glochidion ellipticum Wight Glochidion assamicum (Müll. Arg.) Hook. f. Wurdack et al. (2004)
17 Glochidion heyneanum var. heyneanum Glochidion velutinum Wight Wurdack et al. (2004)
18 Glochidion khasicum (Müll. Arg.) Hook.f. - Wurdack et al. (2004)
19 Glochidion nubigenum Hook. f. - Wurdack et al. (2004)
20 Glochidion oblatum Hook.f. - Wurdack et al. (2004)
21 Glochidion sphaerogynum (Müll.Arg.) Kurz - Wurdack et al. (2004)
22 Phyllanthus clarkei Hook.f. - Wurdack et al. (2004)
23 Phyllanthus debilis J.G.Klein ex Willd. - Wurdack et al. (2004)
24 Phyllanthus emblica L. - Wurdack et al. (2004)
25 Phyllanthus glaucus Wall. ex Müll. Arg. - Wurdack et al. (2004)
26 Phyllanthus leschenaultii Müll. Arg. - Wurdack et al. (2004)
27 Phyllanthus parvifolius Buch.-Ham. ex D. Don - Wurdack et al. (2004)
28 Phyllanthus reticulatus Poir. - Wurdack et al. (2004)
29 Phyllanthus sikkimensis Müll. Arg. - Wurdack et al. (2004)
30 Phyllanthus stylosus Griff. Phyllanthus griffithii Müll. Arg. Wurdack et al. (2004)
31 Phyllanthus urinaria L. - Wurdack et al. (2004)
32 Phyllanthus virgatus G. Forst. - Wurdack et al. (2004)
Putranjivaceae
1 Drypetes assamica (Hook.f.) Pax & K. Hoffm. - Wurdack et al. 2004
2 Drypetes indica (Müll.Arg.) Pax & K. Hoffm. - Wurdack et al. 2004
*

In the Flora of Bhutan by Grierson and Long (1987), some plant species were treated as separate entities, but recent taxonomic revisions have consolidated these into single accepted names.

Acalypha spiciflora Burm.f. (synonym: Cleidion spiciflorum (Burm.f.) Merr), reported by Grierson and Long (1987), has been excluded from the list as it is considered an unresolved name in Plants of the World Online.