Panax siamensis J. Wen, a new species of the ginseng genus (Panax, Araliaceae) from northern Thailand

Jun Wen; Gary Krupnick; Hans-Joachim Esser

doi:10.3897/phytokeys.234.106289

Abstract

We herein describe a new species, Panax siamensis J. Wen, from the tropical monsoon forests in northern Thailand. Panax siamensis is characterized by a combination of characters including horizontally elongated rhizomes with thick internodes, 3–5 whorled leaves each with 7–9 sessile and lanceolate leaflets, lanceolate bracteoles not persisting at the fruiting stage, 2-locular ovaries, and red fruits with a black top. The new species is most closely related to Panax zingiberensis C.Y. Wu & Feng from southeastern Yunnan province of China, sharing the character of sessile leaflets, but differing in that P. siamensis has well developed, elongated rhizomes (vs. compact, ginger-like rhizomes and rootstock in P. zingiberensis), and 7–9 leaflets (vs. (3–) 5–7 leaflets in P. zingiberensis). We also compare Panax siamensis to other related Asian Panax species, including P. assamicus Banerjee, P. bipinnatifidus Seem., P. pseudoginseng Wallich, and P. vietnamensis Ha & Grushv. The new taxon is preliminarily assessed as Vulnerable (VU D2), according to the IUCN Red List criteria. A taxonomic key is provided to facilitate the identification of P. siamensis and its close allies.

Key words

Araliaceae, conservation, ginseng genus, Panax, Panax siamensis J. Wen

Introduction

Panax L., the ginseng genus, is an economically important lineage with several medicinally significant species, e.g., Panax ginseng C.A.Meyer (ginseng), P. quinquefolius L. (American ginseng), P. notoginseng (Burkill) F. H. Chen ex C. Y. Wu et al. (sanchi), P. zingiberensis C.Y. Wu & Feng (ginger-like sanchi), and P. vietnamensis Ha & Grushv. (Vietnamese ginseng) (Zhou et al. 1975; Ha and Grushvitzky 1985; Wen and Zimmer 1996). The genus consists of c. 18 species disjunctly distributed in eastern Asia to the Himalayas and eastern North America, showing a classical eastern Asian – eastern North American biogeographic disjunction (Wen and Zimmer 1996; Wen 1999, 2001; Lee and Wen 2004; Zuo et al. 2015). It is one of the c. 50 genera of the ginseng family Araliaceae (Wen et al. 2001; Plunkett et al. 2018; Gallego‐Narbón et al. 2022).

In spite of its economic (Hu 1976; Proctor 1996) and biogeographic (Wen 1999; Zuo et al. 2017) importance, the species delimitation of Asian Panax has been controversial, largely involving the circumscription of Panax japonicus C.A. Meyer and Panax pseudoginseng Wallich (Li 1942; Hara 1966, 1971; Zhou et al. 1975; Hoo and Tseng 1978; Yang 1981; Xiang and Lowry 2007). Molecular phylogenetic analyses have strongly suggested that Panax japonicus is endemic to Japan and forms a clade with two of the medicinally important species: Panax ginseng and P. quinquefolius (Wen and Zimmer 1996; Lee and Wen 2004; Zuo et al. 2011, 2017). A number of studies have supported the distinctiveness of Panax pseudoginseng as a species that is narrowly distributed in Nepal and adjacent areas of Xizang, China, and as closely related to Panax stipuleanatus Tsai & Feng, which is from southwestern China and northern Vietnam (Lee and Wen 2004; Zuo et al. 2011, 2017). Zhou et al. (1975) also described Panax zingiberensis from southeast and southern Yunnan that has ginger-like roots persistent in older plants, and leaflets without petiolules.

During our revisionary studies of Panax, we discovered a new species from northern Thailand. This species had been recognized as Aralia pseudoginseng (Wallich) Benth. ex C. B. Clarke var. angustifolia (Burkill) Craib (Craib 1931). Hara (1971) and more recently Esser and Jebb (2019) treated it in the genus Panax [as P. pseudoginseng Wallich var. angustifolius (Burkill) H. L. Li], which has been treated as Panax bipinnatifidus Seem. (Zuo et al. 2015, 2017). The new species is highly distinct from Panax bipinnatifidus and several related species from Asia (see Discussion below).

Material and methods

Descriptions and measurements of morphological characters of the new species were based on field observations of living plants and herbarium specimens at A, BKF, CMUB, E, K and US. For comparative studies with other Panax species, we examined herbarium specimens from the following herbaria: A, ABD, ASSAM, B, BKF, BM, BSHC, C, CAL, CAS, CMUB, E, GH, IBSC, K, KATH, K-W, KUN, L, LBG, LE, MO, NBU, NY, P, PE, PH, TCD, TI, U, UC, US, W, WH, and WU (abbreviations following Thiers 2020). We also examined images of type specimens and other herbarium specimens on JSTOR Global Plants (http://plants.jstor.org), the Chinese Virtual Herbarium Website (http://www.cvh.ac.cn/), and National Specimen Information Infrastructure (http://www.nsii.org.cn/).

Taxonomic treatment

Panax siamensis J. Wen, sp. nov.

urn:lsid:ipni.org:names:77328210-1

Figs 1, 2

Type

Thailand. Chiang Mai. A southerly ridge of Doi Pa Mawn, an easterly spur of Doi Angka (i.e., Doi Inthanon), ca. 1350 m, berries bright red with a black top, 30 Dec 1926, in fr, H. B. G. Garrett 364 (holotype: BKF!; isotypes: ABD!, C!, E!, K!, TCD!).

Figure 1.

Illustration of Panax siamensis J. Wen based on J. Wen 7371 (US) A habit B horizontal rhizome with base of stem C leaflet margin D leaflet abaxial surface E infructescence F enlarged infructescence G bracteoles subtending pedicels at flowering stage H older flowers after petals falling off, showing 2-locular ovary I young fruiting stage J seed K seed surface.

Diagnosis

Rhizomes horizontally elongated with thick internodes. Leaves 3—5 at the tip of stem, exstipulate, with 7–9 leaflets; leaflets sessile or nearly so, tapering toward the base, lanceolate, long acuminate at apex, long acute at base, serrulate to doubly so at margin, membranaceous, bristly along veins and veinlets on both surfaces. Ovary 2-locular. Fruits subglobose, bright red with a black top, persistent stigmas recurved, 1–2 seeded, 5–6 mm long, 7–8 mm wide, 3–3.5 mm thick. Seeds ovate, 5–5.5 mm long, 3–4 mm wide, 2.5–3.5 mm thick, surface rough.

Figure 2.

Field images of Panax siamensis and its habitat A habitat in monsoon evergreen forest B infructescence showing red fruits with a black top C habit. Photo credit: A (Ricky Ward), B, C (Jun Wen).

Description

Perennial herb, 60–70 cm, hermaphrodite. Rhizomes horizontally elongated with thick internodes, brown outside, whitish inside; stems light green, 30–45 cm. Leaves 3–5 at the tip of the stem, with 7–9 leaflets, exstipulate, petioles 7–11 cm, glabrous; leaflets sessile or nearly so, tapering toward the base, lanceolate, basal leaflets 7–10 cm long, 2–2.5 cm wide, upper leaflets 13–17.5 cm long, 2–3 cm wide, long acuminate at apex, long acute at base, serrulate to doubly so at margin, membranaceous, bristly along veins and veinlets on both surfaces, bristles or setae 1–2.5 mm long, lateral veins 17–25 per side. Inflorescence consisting of a terminal umbel, sometimes with 1–2 lateral umbels, peduncle 15–20 cm, glabrous, terminal umbels with 70–90 flowers, lateral umbels with 20–30 flowers; pedicels puberulent to slightly so, pale light green, with dark violet color at both ends at late flowering to fruiting stage, 10–13 mm in terminal umbels, 6–8 mm in lateral umbels; bracteoles lanceolate, membranaceous, glabrous, 1.3–1.6 mm long, 0.2–0.3 mm wide, mostly not persistent at fruiting stage. Sepals 5, triangular, 0.4–0.5 mm long, 0.6–0.7 mm wide; petals light green, 1.6–2 mm long, 1–1.1 mm wide; anthers white, filaments pale light green, 2–2.2 mm; ovary 2-locular, stigma white. Fruits subglobose, bright red with a black top, persistent stigmas recurved, 1–2 seeded, 5–6 mm long, 7–8 mm wide, 3–3.5 mm thick. Seeds ovate, 5–5.5 mm long, 3–4 mm wide, 2.5–3.5 mm thick, surface rough.

Additional specimens examined

Thailand. Chiang Mai: Mae Soi Ridge, Mae Soi Subdistrict, near Ban Bah Cluary (Meo Village), 1475 m, 11 Aug 1991, in fl, shaded place, mixed evergreen hardwood and pine forest, J. F. Maxwell 91-722 (A, CMUB, E); Ob Luang National Park, Mae Soi Conservation Area, Bah Gluay (Hmong) village area, between the Ranger Station and the village, on the N side of the road passing through the Bah Gluay village, elev. 1550 m, evergreen forest, plant c. 60–70 m tall, fruits red with a black top, 04 Nov 2003, fr, J. Wen 7371 (KUN, US).

Phenology

Flowering in August; fruiting in November to December.

Distribution

Northern Thailand; elevation 1350–1550 m.

Ecology

In shaded areas of monsoon evergreen hardwood forests, or in mixed evergreen hardwood and pine forests, granite bedrock.

Etymology

The species epithet denotes the geographic distribution of the species in Thailand.

Conservation

The area of occupancy (AOO) of this species as measured with a 2×2 grid is estimated to be 12 km²; the extent of occurrence (EOO) is estimated to be 39.54 km². Apart from habitat destruction, no specific threats are known. It is not found in cultivation, and it is not known from any ex situ collections. With a restricted area of occupancy, only three known locations, and a plausible future threat due to stochastic events or habitat disturbance brought about by human activities near villages, Panax siamensis is preliminarily assessed with a status of Vulnerable (VU D2) according to IUCN Red List Criteria (IUCN 2012, 2022).

Discussion

The new species Panax siamensis is distinguished from other Panax species by a combination of characters including horizontally elongated rhizomes with thick internodes, 3–5 whorled leaves each with 7–9 sessile and lanceolate leaflets, lanceolate bracteoles not persisting at the fruiting stage, 2-locular ovaries, and red fruits with a black top. The new taxon is sister to Panax zingiberensis from southeastern Yunnan province of China (J. Wen, unpublished), sharing the character of sessile leaflets. The two species differ in that P. siamensis has elongated rhizomes (vs. compact ginger-like rhizomes in P. zingiberensis), and 7–9 leaflets (vs. 5–7 leaflets in P. zingiberensis). As P. zingiberensis is medicinally important (Zhou et al. 1975), it is important to explore the chemistry of P. siamensis to test its medicinal value.

Panax siamensis is similar to Panax vietnamensis from Vietnam and southwestern China in that both species have bamboo-like horizontally elongated rhizomes and 2-locular ovaries. They can be easily differentiated in that P. vietnamensis usually has 5 (–7) leaflets (vs. 7–9 leaflets in P. siamensis) that are ovate to elliptic (vs. lanceolate in P. siamensis), petiolules 8–15 mm long (vs. sessile leaflets without conspicuous petiolules in P. siamensis), and glandular pedicels (puberulent pedicels in P. siamensis) (Ha and Grushvitzky 1985; Wen 2001; Duy et al. 2016).

Even though Panax siamensis was recently treated as part of P. pseudoginseng (Esser and Jebb 2019), the new species is highly distinct from Panax pseudoginseng, which is narrowly distributed in Nepal and neighboring Xizang of China (Wallich 1829; Wen 2001). Panax pseudoginseng has fusiform tubers that are single or fascicled (vs. tubers absent in P. siamensis), rhizomes short and upright (vs. elongate and horizontal in P. siamensis), leaves with stipules (stipules absent in P. siamensis), and fruits that are red throughout (vs. fruits red with a black top in P. siamensis) (Wen 2001; Yoo et al. 2001).

Panax pseudoginseng var. angustifolius is now considered as part of Panax bipinnatifidus Seem. (Wen 2001; Zuo et al. 2015). Burkill (1902) originally described Aralia quinquefolia var. angustifolia Burkill as a taxon from the Sikkim, Bhutan and Khasia Hills (Assam), citing specimens belonging to two species, P. bipinnatifidus Seem. and P. assamicus R.N. Banerjee. Panax siamensis resembles P. assamicus in the lanceolate leaflets that are sessile or nearly so. They differ in that P. assamicus has mostly 5 (–7) leaflets (vs. 7–9 leaflets in P. siamensis), persistent bracteoles (vs. bracteoles mostly not persisting in fruiting stage in P. siamensis), pilose pedicels (vs. puberulent pedicels with extremely short hair-like structures in P. siamensis), oblong sepals (vs. triangular sepals in P. siamensis), and 2—3 (–4) locular ovaries (vs. 2-locular ovaries in P. siamensis). Panax assamicus is also a much taller herbaceous species that is 70–150 cm tall (vs. P. siamensis 60–70 cm tall). Their habitats are also highly distinctive, with P. siamensis in tropical monsoon forests and P. assamicus in temperate deciduous or mixed forests.

Panax siamensis can be easily distinguished from P. bipinnatifidus in that the latter has horizontal rhizomes with slender internodes and subglobose nodes (vs. horizontal rhizomes with thick and short internodes, i.e., bamboo-like, in P. siamensis), leaves with 5 (–7) leaflets (vs. 7–9 leaflets in P. siamensis), and terminal umbels with fewer flowers (25–50 flowers in P. bipinnatifidus, vs. 70–90 flowers in P. siamensis). Ecologically, Panax bipinnatifidus occurs in deciduous or mixed deciduous and coniferous forests in western China to the Himalayas at higher elevations of 2000–3600 m (Wen 2001), while P. siamensis occurs in monsoon evergreen hardwood forests, or in mixed evergreen hardwood and pine forests around 1350–1550 m.

We herein provide a key to Panax siamensis and its close allies to help differentiate the species.

Key to Panax siamensis and its close congeneric allies

1	Rhizomes elongate and creeping; fruits red with a black top	2
–	Rhizomes short and upright; fruits red throughout	8
2	Rhizomes with slender internodes and subglobose nodes	*P. bipinnatifidus*
–	Rhizomes with short and thick internodes	3
3	Leaflets usually with petiolules	4
–	Leaflets usually without petiolules	6
4	Leaves subtended by stipules, leaflets usually divided at the margin	*P. stipuleanatus*
–	Leaves without stipules, leaflets usually undivided, only occasionally divided	5
5	Leaves with 5 (rarely 3 or 7) leaflets, leaflets oblong or ovate, occasionally lanceolate, light green; ovaries 2-locular	*P. vietnamensis*
–	Leaves with 7–9 (rarely 5) leaflets, leaflets lanceolate to narrowly so, dark green; ovaries 2—4-locular	*P. wangianus*
6	Roots ginger-like, persistent in older plants; leaflets elliptic to obovate	*P. zingiberensis*
–	Roots tuberous, decayed in older plants; leaflets lanceolate	7
7	Plant 70–150 cm tall; leaflets usually 5 to occasionally 7; bracteoles subtending pedicels persistent into fruiting stage; ovaries 2—3 (–4) –locular	*P. assamicus*
–	Plant 60—70 cm tall; leaflets 7—9; bracteoles subtending pedicels mostly not persisting at fruiting stage; ovaries 2—locular	*P. siamensis*
8	Roots singly, sometimes forked; stipules linear in shape; each umbel mostly with 80–100 flowers	*P. notoginseng*
–	Roots usually fascicled; stipules ovate in shape; each umbel mostly with 40–65 flowers	*P. pseudoginseng*

Acknowledgements

We thank the following herbaria (A, ASSAM, B, BKF, BM, BSHC, CAL, CAS, CMUB, E, GH, IBSC, K, KATH, K-W, KUN, L, LBG, LE, MO, NBU, NY, P, PE, PH, TI, U, UC, US, W, WH, and WU) for allowing the examination of their specimens, Robin Everly for assistance with obtaining literature, Alice Tangerini for preparing the illustration, J.F. Maxwell and Ricky Ward for field assistance and their warm friendship, and Greg Plunkett and Pedro Fiaschi for their constructive comments on the manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

No funding was reported.

Author contributions

All authors have contributed equally.

Author ORCIDs

Jun Wen https://orcid.org/0000-0001-6353-522X

Gary Krupnick https://orcid.org/0000-0002-1357-4826

Hans-Joachim (Hajo) Esser https://orcid.org/0000-0001-6518-8612

Data availability

All of the data that support the findings of this study are available in the main text or Supplementary Information.

References

Burkill IH (1902) Ginseng in China. Bulletin of Miscellaneous Information. Royal Gardens, Kew 1902: 4–11. https://doi.org/10.2307/4114308

Craib WG (1931) Flora Siamensis Enumeratio. Vol. 1. Bangkok: Siam Society.

Duy NV, Trieu LN, Chinh ND, Tran VT (2016) A new variety of Panax (Araliaceae) from Lam Vien Plateau, Vietnam and Its molecular evidence. Phytotaxa 277(1): 47–58. https://doi.org/10.11646/phytotaxa.277.1.4

Esser H-J, Jebb MHP (2019) Araliaceae. In: Balslev H, Chayāmarit K (Eds) Flora of Thailand 14(2). Bangkok: Forest Herbarium, Department of National Parks, Wildlife and Plant Conservation, 185–251.

Gallego‐Narbón A, Wen J, Liu J, Valcárcel V (2022) Hybridization and genome duplication for early evolutionary success in the Asian Palmate group of Araliaceae. Journal of Systematics and Evolution 60(6): 1303–1318. https://doi.org/10.1111/jse.12906

Ha DT, Grushvitzky IV (1985) A new species of the genus Panax (Araliaceae) from Vietnam. Botanicheskii Zhurnal 70: 519–522.

Hara H (1966) The flora of eastern Himalaya. Tokyo: The University of Tokyo Press.

Hara H (1971) The flora of eastern Himalaya. Second Report. Tokyo: The University of Tokyo Press.

Hoo G, Tseng CJ (1978) Araliaceae. In: Hoo G, Tseng CJ (Eds) Flora Reipublicae Popularis Sinicae. Beijing: Science Press, Beijing. 54: 1–190.

Hu SY (1976) The genus Panax (ginseng) in Chinese medicine. Economic Botany 30(1): 11–28. https://doi.org/10.1007/BF02866780

IUCN (2012) IUCN Red List Categories and Criteria, Version 3.1 (2^nd edn.). Gland and Cambridge, 32 pp.

IUCN (2022) The IUCN Red List of Threatened Species. Version 2022-2. https://www.iucnredlist.org/

Lee CH, Wen J (2004) Phylogeny of Panax using chloroplast trnC-trnD intergenic region and the utility of trnC-trnD in interspecific studies of plants. Molecular Phylogenetics and Evolution 31(3): 894–903. https://doi.org/10.1016/j.ympev.2003.10.009

Li HL (1942) The Araliaceae of China. Sargentia 2: 1–134. https://doi.org/10.5962/p.265316

Plunkett GM, Wen J, Lowry PP, Mitchell AD, Henwood MJ, Fiaschi P (2018) Araliaceae. In: Kadereit JW, Bittrich V (Eds) Flowering Plants. Eudicots. The Families and Genera of Vascular Plants. Berlin: Springer. 15: 413–446. https://doi.org/10.1007/978-3-319-93605-5_4

Proctor JTA (1996) Ginseng: old crop, new directions. In: Janick J (Ed.) Progress in New Crops, Proceedings Third National Symposium, New Crops: new opportunities, new technologies. Alexandria, Virginia: ASHS Press, 565–577.

Thiers B (2020) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s virtual Herbarium. http://sweetgum.nybg.org/ih/

Wallich N (1829) An account of the Nipal ginseng. Transactions of the Medical and Physical Society of Calcutta 4: 115–120.

Wen J (1999) Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annual Review of Ecology and Systematics 30(1): 421–455. https://doi.org/10.1146/annurev.ecolsys.30.1.421

Wen J (2001) Species diversity, nomenclature, phylogeny, biogeography, and classification of the ginseng genus (Panax L., Araliaceae). In: Punja ZK (Ed.) Proceedings of the International Ginseng Workshop — utilization of biotechnological, genetic & cultural approaches for North American & Asian ginseng improvement. Simon Fraser University, Canada, 67–88.

Wen J, Zimmer EA (1996) Phylogeny and biogeography of Panax L. (the ginseng genus, Araliaceae): Inferences from ITS sequences of nuclear ribosomal DNA. Molecular Phylogenetics and Evolution 6(2): 167–177. https://doi.org/10.1006/mpev.1996.0069

Wen J, Plunkett GM, Mitchell AD, Wagstaff SJ (2001) The evolution of Araliaceae: A phylogenetic analysis based on ITS sequences of nuclear ribosomal DNA. Systematic Botany 26: 144–167.

Xiang QB, Lowry PL (2007) Araliaceae. In: Wu ZY, Raven PH, Hong DY (Eds) Flora of China. Beijing: Science Press & St. Louis: Missouri Botanic Garden Press 13: 435–491.

Yang D-Q (1981) The cyto-taxonomic studies on some species of Panax L. Zhiwu Fenlei Xuebao 19: 298–303.

Yoo K-O, Malla KJ, Wen J (2001) Chloroplast DNA variation of Panax (Araliaceae) in Nepal and its taxonomic implications. Brittonia 53(3): 447–453. https://doi.org/10.1007/BF02809800

Zhou J, Huang WG, Wu MZ, Yang CR, Feng KM, Wu CY (1975) Triterpenoids from Panax Linn. and their relationship with taxonomy and geographical distribution. Acta Phytotaxomica Sinica 13(2): 29–45. [pls. 6–7]

Zuo Y-J, Chen Z-J, Kondo K, Funamoto T, Wen J, Zhou S-L (2011) DNA barcoding of Panax species. Planta Medica 77(02): 182–187. https://doi.org/10.1055/s-0030-1250166

Zuo Y-J, Wen J, Ma J-S, Zhou S-L (2015) Evolutionary radiation of the Panax bipinnatifidus species complex (Araliaceae) in the Sino-Himalayan region of eastern Asia as inferred from AFLP analysis. Journal of Systematics and Evolution 15(3): 210–220. https://doi.org/10.1111/jse.12119

Zuo Y-J, Wen J, Zhou S-L (2017) Intercontinental and intracontinental biogeography of the eastern Asian – eastern North American disjunct Panax (the ginseng genus, Araliaceae), emphasizing its diversification processes in eastern Asia. Molecular Phylogenetics and Evolution 117: 60–74. https://doi.org/10.1016/j.ympev.2017.06.016

﻿Abstract