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Research Article
Thismia malayana (Thismiaceae), a new mycoheterotrophic species from Peninsular Malaysia
expand article infoMat Yunoh Siti-Munirah, Chin Hardy-Adrian§, Sharipudin Mohamad-Shafiq|, Zainuddin Irwan-Syah|, Abd Halim Hamidi
‡ Forest Research Institute Malaysia, Kepong, Malaysia
§ Unaffiliated, Seremban, Malaysia
| Unaffiliated, Jerantut, Malaysia
¶ Jabatan Perhutanan Negeri Sembilan, Seremban, Malaysia
Open Access

Abstract

A new species of the mycoheterotrophic genus Thismia from Malaysia is described and illustrated. Thismia malayana introduced here was found in two localities: in the lowlands of Gunung Angsi Forest Reserve, Negeri Sembilan, and in the hilly dipterocarp forests of Gunung Benom in Tengku Hassanal Wildlife Reserve, Pahang. Thismia malayana falls into the section Thismia subsect. Odoardoa, as it has creeping vermiform roots and free equal tepals. It is characterised by the following taxonomically important features: a sepia-brown, urceolate-curved floral tube, free equal tepals with terminal appendages, prominent bright yellow annulus and bright violet-blue stamens each bearing five appendages (one pair of club-shaped inwards-pointing, one pair of acute outwards-pointing, and one central appendage). According to the categories and criteria of the IUCN Red List, T. malayana is provisionally classified as Vulnerable.

Key words

Negeri Sembilan, new species, Pahang, Thismia subsect. Odoardoa, vulnerable

Introduction

The tropical rainforests of Southeast Asia together form the second largest area of tropical rainforests in the world. Also, the tropical lowland evergreen rainforest is the most species-rich forest formation in the region and structurally the most complex one, with species composition varying according to local soil and drainage conditions (Davis et al. 1995). Native plants of this type of forest include Thismia Griff., a genus of non-photosynthetic, mycoheterotrophic plants belonging to the family Thismiaceae. The genus Thismia comprises around 100 currently recognised species, and its range extends across various regions of the world, including tropical and subtropical Asia, northern and eastern Australia to New Zealand, the north-central USA, Costa Rica and southern tropical America (POWO 2024).

One of the most remarkable characteristics of Thismia is its mycoheterotrophic way of life. Unlike most plants, its species do not produce chlorophyll and are not capable of photosynthesis. A mycoheterotrophic plant is in fact a parasite of the mycorrhizal symbiosis, cheating it of the carbon resources that are shared in the mycorrhizal symbiosis, and this adaptation allows it to survive in the undergrowth of forests where the light availability is low (Merckx 2013; Watkinson 2016). Thismia species are known for their small size, which is usually only a few centimeters (Leake 1994). They are typically hidden in leaf litter and grow near tree roots or old rotten logs. Despite their small size, they are very sensitive to environmental changes, e.g. they decay easily when pulled out of its original habitat. Thismia species exhibit a number of unusual morphological features that continue to fascinate due to their amazing diversity of flower shapes and colours (Feller et al. 2022). The flower structure of Thismia is highly specialised to pollination by fungus gnats or other small insects (Thorogood and Siti-Munirah 2021). The flowers often have a complex shape with cup-like or spherical structures and intricate patterns that presumably attract pollinators. Due to their cryptic appearance, many Thismia species are still poorly known in terms of taxonomy and other biological aspects.

Another Thismia species is described here that is new to science. It was first discovered in 2020 in the Tengku Hassanal Wildlife Reserve (WR) (formerly known as Krau Wildlife Reserve) in the state of Pahang in Malaysia. It was later found also in a forested area in Ulu Bendul Recreation Park (RP), a popular nature and recreation area in Negeri Sembilan, Malaysia. It is located near the town of Kuala Pilah, about 25 kilometres from Seremban. The Ulu Bendul RP is also part of the Gunung Angsi Forest Reserve (FR) and offers nature lovers, hikers and explorers the opportunity to immerse themselves in the beauty of the tropical rainforest and discover its rich flora and fauna as well as its contribution to wildlife conservation. The type material of the new species was collected in February 2023 at the edge of the Gunung Angsi main trail in the forest area of Ulu Bendul RP.

Materials and methods

The specimens of the new species were collected from both localities (Map 1), preserved in 70% ethanol and deposited in the Kepong Herbarium (KEP). Morphological characters were examined, and measurements were made using an Olympus SZ61 stereomicroscope and high-resolution macrophotography of fresh and preserved material. The morphology of the new species was carefully compared with all related species of the genus Thismia. Assessment of the conservation status according to the categories and criteria of the IUCN Red List (IUCN Standards and Petitions Committee 2022).

Map 1. 

Distribution of Thismia malayana (black circle) in Peninsular Malaysia: the type locality in Ulu Bendul RP, Gunung Angsi FR in the state of Negeri Sembilan and the Tengku Hassanal WR, Temerloh in the state of Pahang.

Taxonomic account

Thismia malayana Siti -Munirah, Hardy-Adrian, Mohamad-Shafiq & Irwan-Syah, sp. nov.

Figs 1, 2, 3

Diagnosis

Thismia malayana resembles T. chrysops but differs by the brown-whitish colour of the floral tube (vs. very dark sepia brown), glabrous surface of the tepal appendages (vs. finely ciliate), presence of transverse bars at inner surface of floral tube (vs. bars absent), supraconnective apex of each stamen with 5 appendages: one pair of club-shaped inwards-pointing, one pair of acute outwards-pointing, and one central appendage (vs. 7 appendages: one pair of club-shaped, one pair of acute and 3 central appendages).

Figure 1. 

Thismia malayana A flowering plant B flower, side view C flower, view from above D flower, longitudinal section E three stamens, outer view F tepal with terminal appendage, adaxial view G ovary, longitudinal section H style and stigma I involucral bract, adaxial view J leaf, adaxial view. All drawn by Mohamad Aidil Noordin from spirit material, Siti-Munirah FRI 101705 (A–C); FRI 101701 (D–J).

Type

Malaysia. Peninsular Malaysia: Negeri Sembilan, Kuala Pilah Distr., Gunung Angsi FR, Ulu Bendul RP, a trail to Gunung Angsi., elevation ca. 206–208 m a.s.l., 9 February 2023. Siti-Munirah FRI 101705 (holotype KEP!, spirit collection, barcode no. SC12021]).

Figure 2. 

Thismia malayana A flowering plant A1 floral tube, inner surface A2 annulus and stamen filaments, view from inside B inflorescence with anthetic flower and several young fruits B1 style and stigma B2 annulus, top view C flower, side view D, E stamens, view from inside and from outside, E1 stamen supraconnectives: one pair of club-shaped inwards-pointing, one pair of acute outwards-pointing, and one central appendage F stamen supraconnectives, apical view G stamen tube, view from below H, H1 fruit after dehiscence, top view, H2 seeds I shoot base with roots. Photos by Siti-Munirah (A1–I) and Hardy-Adrian (A) from FRI 101701 (A), FRI 101702 (F, G, I), FRI 101703 (E1), FRI 101705 (B, B2, H, H1, H2) & FRI 101710 (A1, A2, B1, C, D, E). Images not to scale (see dimensions in description and Figs 1, 3).

Description

Achlorophyllous herb, up to 10 cm tall, predominantly glabrous. Roots vermiform, unbranched, ca. 1 mm in diameter, light brown. Stem erect, up to ca. 6 cm long, 0.2 cm in diameter, pale brownish, bearing 1–4 flowers. Leaves 2–4, alternate, distant, triangular to narrowly triangular, scale-like, apex acute, margin slightly irregularly serrate (almost entire), 6 mm long, ca. 1 mm wide at base, pale brown. Involucral bracts 3, spirally/alternately arranged, similar to leaves but slightly larger, triangular to narrowly triangular, scale-like, apex acute, margin entire, 8 mm long, ca. 1.5–2.5 mm wide at base, pale brown or pale orange. Pedicel ca. 2 mm long at anthesis, elongating to ca. 5 cm long after anthesis, pale brown. Flowers terminal, asymmetrical, slightly zygomorphic, ca. 13 mm long (including ovary). Floral tube urceolate-curved, ca. 7 mm long, ca. 5 mm wide at middle, ca. 4 mm wide at base, sigmoidally bent in lower part; outer surface brown to whitish-sepia (whitish proximally & brown distally), with 12 longitudinal ribs orangish proximally & dark brown distally; inner surface reticulate, with whitish transverse bars, of similar color as outer surface. Tepals 6, free, triangular to ovate, apex acute, up to ca. 2.5 mm long, ca. 1.5–2.6 mm wide at base, dark brown, apically bearing a tentacle-like appendage; appendage narrowing towards apex, each equal in length up to ca. 6 mm long, 0.5 mm wide, whitish towards apex, becoming brownish with age. Annulus moderately raised, ring-shaped, ca. 5.4 mm in diameter, with ring width ca. 1.2 mm, orange, becoming bright yellow with age, aperture ca. 3.2 mm in diameter. Stamens 6, pendent from annulus; filaments free, ca. 1 mm long, curved downwards, yellowish to whitish; anther ca. 0.7 mm long; connectives and supraconnectives narrow at base (ca. 1.5 mm wide) and broad at apex (ca. 2 mm wide), with outer side bluish to violet; inner side bluish, violet, whitish to yellowish, flattened at inner surface, laterally connate to form a tube, ca. 4.5 mm long, supraconnective apex with one pair of club-shaped inwards-pointing, ca. 0.8–1 mm long and one pair of acute outwards-pointing ca. 0.3 mm long appendages, and one central appendage ca. 0.5–0.6 mm long; supraconnective bearing a skirt-like lateral appendage at outer side protruding towards inner side of floral tube, bearing trichomes at both sides; lateral appendage not exceeding the tip of the supraconnective appendages, margin lobed with translucent trichomes; interstaminal glands inserted on the line of fusion between supraconnectives at the level of attachment of lateral appendages, bluish (concolorous with supraconnectives). Ovary inferior, unilocular; placentas 3, free, column-like, arising from the bottom of the ovary; ovules numerous. Style ca. 0.74 mm long, dark blackish; stigma ca. 0.85 mm long, papillose, 3-lobed, with lobes ± rectangular and bifurcate at apex, dark blackish. Fruit dehiscent, cup-shaped, 6 mm in height, 6–8 mm in diameter, pale white to creamy. Seeds long oval, ca. 0.38–0.41 mm long, ca. 0.15–0.17 mm wide.

Additional specimens examined

Malaysia. Peninsular Malaysia: Negeri Sembilan, Kuala Pilah District, Gunung Angsi FR, Ulu Bendul RP, elev. ca. 206–208 m, February 2023, Siti-Munirah, FRI 101701 (KEP), FRI 101702 (KEP), FRI 101703 (KEP), FRI 101704 (KEP) FRI 101709 (KEP), FRI 101710 (KEP), FRI 101711 (KEP); Pahang, Temerloh District, Tengku Hassanal WR, elev. ca. 200 m, 31 December 2020, Mohamad-Shafiq & Irwan-Syah, FRI 91126 (KEP).

Figure 3. 

Thismia malayana with scales (the finest grade is 0.5 mm) A side view B top view C the size compared to the 20-sen coin (23.59 mm in diameter). Photos by Hardy-Adrian from uncollected plants.

Distribution

Endemic to Peninsular Malaysia. Recorded in two localities: one in Gunung Angsi FR in Negeri Sembilan state and another in Tengku Hassanal WR in Pahang state (Fig. 4).

Figure 4. 

Habitat (in situ) of Thismia malayana in Ulu Bendul RP in Gunung Angsi FR (A, B) and the Tengku Hassanal WR (C–E) A Thismia malayana at its habitat, which is located right next to the main trail to Gunung Angsi B Siti-Munirah showing the habitat of T. malayana C path to Lata Bujang and Gunung Benom D the plants growing on rotten wood E Mohamad-Shafiq observed a Thismia malayana in its habitat. Photos by Siti-Munirah (A, B) and Mohamad-Shafiq (C–E).

Ecology

In medium-moist or mesic, shady areas of lowland dipterocarp forests at elevations of 200–450 m a.s.l. Flowering and fruiting usually from December to February but flowering also observed in June. According to the third and fourth author’s observations, T. malayana was only sighted and observed a few times a year, especially during the rainy season.

Etymology

The specific epithet malayana is derived from Malaya, a name formerly used for Peninsular Malaysia. The epithet refers to the known region of the species distribution.

Conservation status

According to the IUCN standards (IUCN 2022), we propose to classify the preliminary conservation status of Thismia malayana as VU (Vulnerable). This particular species has only been found in two locations. One of the sites is located in a protected area (Tengku Hassanal WR), the other in a water catchment forest under the PRF class protection forest (Gunung Angsi FR), which also includes Ulu Bendul RP. Both habitats are therefore considered stable. However, the population of this species was detected near a hiking trail at both sites, which exposes this species to the risk of trampling due to its small size. During the survey conducted between 2022 and 2023, only less than 10 individuals were found. However, due to the limited time and area of the survey and also mycoheterotrophic nature of the species which remains hidden in the soil for most of its life, it was not possible to determine the estimated number of mature individuals in the population. Therefore, this species is classified as Vulnerable based on criterion D2.

Notes

According to the classifications of Jonker (1938) and Kumar et al. (2017), T. malayana is placed in subgenus Thismia section Thismia subsection Odoardoa Schltr. (Schlechter 1921), as it has six free, equal tepals and vermiform roots. Among the Thismia subsection Odoardoa, the following species share the curved or bent floral tube characteristic of T. malayana: T. chrysops from Johor (Gunung Ledang, Peninsular Malaysia) (Ridley 1895), T. cornuta from Sarawak (Malaysia) (Hroneš et al. 2018), T. inconspicua from Brunei (Sochor et al. 2017) and T. kinabaluensis from Sabah (Malaysia) (Nishioka et al. 2018). A detailed morphological comparison of T. malayana and these morphologically most similar four species is presented in Table 1.

Table 1.

Morphological comparison of T. malayana with T. chrysops (Ridley 1895), T. cornuta (Hroneš et al. 2018), T. kinabaluensis (Nishioka et al. 2018) and T. inconspicua (Sochor et al. 2017).

Characteristics T. malayana T. chrysops T. cornuta T. inconspicua T. kinabaluensis
Floral tube
Outer
colour brown to whitish-sepia very dark sepia brown translucent-white (light) brownish brown or beige
colour of longitudinal ribs
upper part dark brown in rose pink pale pinkish sepia-brown light brown or beige streaks
lower part orangish chocolate-brown pale pinkish both ribs and background gradually darkening toward the apex of the same colour as the floral tube
Inner
transverse bars present absent absent absent present
Annulus
colour bright yellow bright yellow pinkish sepia-brown on the outer margin, brownish-orange to light orange on the inner margin and grayish in between with blue circle on the outer margin, orange to yellow on the inner margin
Tepal
colour dark brown bright sienna, brown/ chocolate brown white sepia-brown pale blue
Appendages
colour brown to whitish bright sienna brown white sepia-brown pale blue
surface glabrous finely ciliate glabrous glabrous glabrous
Stamens
colour bluish, violet, whitish, yellowish unknown translucent-white translucent-white translucent-white
appendages of supraconnectives 5 (2 club-shaped pointing centripetally, 2 acute pointing centrifugally and 1 central appendage) several, (2 club-shaped and few shorter ones) 2 club-shaped 4 (2 club and 2 tooth-shaped) 3 (1 filiform between 2 club-shaped)

Acknowledgements

We thank the Jabatan Perhutanan Negeri Sembilan (JPNNS) and Jabatan Perhutanan Semenanjung Malaysia (JPSM) for permission to conduct a botanical collection, Jabatan Perlindungan Hidupan Liar dan Taman Negara (PERHILITAN) and Persatuan Pemandu Pelancong Mukim Ulu Cheka (PAMUC) for deposited specimen from Tengku Hassanal WR to Kepong Herbarium (KEP). We would like to thank the staff of Ulu Bendul RP for their assistance and Angan Atan for his help during the fieldwork. We would like to thank all reviewers, Michal Hroneš, Michal Sochor, Martin Dančák and Maxim Nuraliev for constructive comments on our manuscript. We thank Mohamad Aidil Noordin for the botanical drawings, Wendy SY Yong for the assistance in conservation status assessment and Mohd Faizal MT for the encouragement and great help in many ways to the first author in the preparation of the manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This research was conducted under the Flora of Peninsular Malaysia Project (FPM) at the Forest Research Institute Malaysia (FRIM), Kepong, funded by the Ministry of Natural Resources and Environmental Sustainability (NRES), under the 12th Malaysian Plan (SPPII No. P23085100018003). Special thanks to the Nagao Research Grant (NEF) for partially funding the Thismia research.

Author contributions

All authors contributed equally to this study and made a significant contribution to the overall result.

Author ORCIDs

Mat Yunoh Siti-Munirah https://orcid.org/0000-0002-5062-9988

Data availability

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

References

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