NATURE IN SINGAPORE 13 Date of Publication: 4 August 2020 … · 2020-08-04 · This paper belongs...

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27 NATURE IN SINGAPORE 2020 13: 2737 Date of Publication: 4 August 2020 DOI: 10.26107/NIS-2020-0004 © National University of Singapore Additions to the Flora of Singapore: New and overlooked records of exotic plant species (3) Lily M. J. Chen 1* , Hock Keong Lua 2 , Regina S. W. Yeo 3 , Le Min Choo 1 , Wei Hao Lim 1 , Parusuraman Athen 1 , Keng Soon Chua 4 , Sin Lan Koh 1 & Boon-Chuan Ho 1 1 Singapore Botanic Gardens, National Parks Board, 1 Cluny Road, Singapore 259569, Republic of Singapore; Email: [email protected] ( * corresponding author) 2 National Biodiversity Centre, National Parks Board, 1 Cluny Road, Singapore 259569, Republic of Singapore 3 Graduate School of Integrated Sciences for Life, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739- 8528, Japan 4 Lee Kong Chian Natural History Museum, National University of Singapore, Singapore 117377, Republic of Singapore Abstract. Four non-native plant species, Acalypha hispida Burm.f., Bixa orellana L., Bryophyllum tubiflorum Harv. and Calotropis gigantea (L.) W.T.Aiton from four families (Apocynaceae, Bixaceae, Crassulaceae and Euphorbiaceae), are added to the Flora of Singapore. Bixa orellana was previously overlooked as its record of naturalisation was listed in grey literature. Two genera, Bixa L. and Calotropis R.Br., and the family Bixaceae, are newly recorded for the Flora of Singapore. Key words. Asclepiadoideae, Nathaniel Cantley, casual, naturalised, new family records, new generic records, Straits Settlement reports INTRODUCTION This paper belongs to a series dealing with the naturalised and casually occurring flora of Singapore to better document its diversity with proper specimen records. 17 species have so far been added to the non-indigenous species list of Singapore in the first two parts of this series (Chen et al., 2018a; Chen et al., 2018b). In this third part, four more species, two genera, and one family are reported here for Singapore as part of this ongoing project. NEW RECORDS OF NATURALISED SINGAPORE PLANTS 1. Acalypha hispida Burm.f. Fl. Ind. 203, t. 61: f. 1 (1768) (Euphorbiaceae) (Fig. 1) Key reference. Sagun et al. (2010). Description. Shrub to c. 1.6 m tall. Leaves alternate; petiole 16.520.5 cm long; lamina simple, 2528.2 × 1519.8 cm; ovate to broadly ovate, margin serrate broadly serrate to ± crenulate, base rounded, obtuse or cuneate, apex attenuate or acuminate, pubescent/glabrous on both surfaces. Staminate inflorescences and flowers not seen (possibly dioecious). Pistillate inflorescences pendent, axillary, densely flowered, appearing bright red from the crowded mass of styles; peduncles 3.56.2 cm long; rachis 42.547 cm long. Pistillate flowers sessile; ovary c. 1 × 1 cm, ± trilobed, densely pubescent; styles 0.60.8 cm long, bright red, ± free at the base, laciniate. Fruits and seeds not seen. Distribution. The exact country of origin is uncertain, but it is thought to be native to the Bismarck Archipelago and Papua New Guinea (Radcliffe-Smith, 1996); it is widely cultivated elsewhere in Malesia, where it has also escaped into surrounding forests (Sagun et al., 2010). Occurrence in Singapore. This species appears to persist in abandoned areas as a remnant from former cultivation. It was previously recorded by Chong et al. (2009) as Cultivated Only. Local status. Casual; it is not known to set seed. This species is possibly dioecious as it is known only from cultivated pistillate plants; there are no records of the staminate plants and perfect flowers, fruits and seeds (Sagun et al., 2010). Plants are propagated exclusively from cuttings. Specimens examined. SINGAPORE: Area near Thomson Nature Park, 29 January 2020, Chen, L.M.J., Lim, W.H., Athen, P., Choo, L.M., Ho, B.C. et al., LCMJ 2020-057 (2 sheets) (SING).

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NATURE IN SINGAPORE 2020 13: 27–37 Date of Publication: 4 August 2020

DOI: 10.26107/NIS-2020-0004 © National University of Singapore

Additions to the Flora of Singapore: New and overlooked records of exotic plant species (3)

Lily M. J. Chen1*, Hock Keong Lua2, Regina S. W. Yeo3, Le Min Choo1, Wei Hao Lim1, Parusuraman Athen1, Keng Soon

Chua4, Sin Lan Koh1 & Boon-Chuan Ho1

1Singapore Botanic Gardens, National Parks Board, 1 Cluny Road, Singapore 259569, Republic of Singapore; Email:

[email protected] (*corresponding author) 2National Biodiversity Centre, National Parks Board, 1 Cluny Road, Singapore 259569, Republic of Singapore 3Graduate School of Integrated Sciences for Life, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-

8528, Japan 4Lee Kong Chian Natural History Museum, National University of Singapore, Singapore 117377, Republic of Singapore

Abstract. Four non-native plant species, Acalypha hispida Burm.f., Bixa orellana L., Bryophyllum tubiflorum Harv. and

Calotropis gigantea (L.) W.T.Aiton from four families (Apocynaceae, Bixaceae, Crassulaceae and Euphorbiaceae), are

added to the Flora of Singapore. Bixa orellana was previously overlooked as its record of naturalisation was listed in grey

literature. Two genera, Bixa L. and Calotropis R.Br., and the family Bixaceae, are newly recorded for the Flora of

Singapore.

Key words. Asclepiadoideae, Nathaniel Cantley, casual, naturalised, new family records, new generic records, Straits

Settlement reports

INTRODUCTION

This paper belongs to a series dealing with the naturalised and casually occurring flora of Singapore to better document

its diversity with proper specimen records. 17 species have so far been added to the non-indigenous species list of

Singapore in the first two parts of this series (Chen et al., 2018a; Chen et al., 2018b). In this third part, four more species,

two genera, and one family are reported here for Singapore as part of this ongoing project.

NEW RECORDS OF NATURALISED SINGAPORE PLANTS

1. Acalypha hispida Burm.f. Fl. Ind. 203, t. 61: f. 1 (1768) (Euphorbiaceae)

(Fig. 1)

Key reference. Sagun et al. (2010).

Description. Shrub to c. 1.6 m tall. Leaves alternate; petiole 16.5–20.5 cm long; lamina simple, 25–28.2 × 15–19.8 cm;

ovate to broadly ovate, margin serrate broadly serrate to ± crenulate, base rounded, obtuse or cuneate, apex attenuate or

acuminate, pubescent/glabrous on both surfaces. Staminate inflorescences and flowers not seen (possibly dioecious).

Pistillate inflorescences pendent, axillary, densely flowered, appearing bright red from the crowded mass of styles;

peduncles 3.5–6.2 cm long; rachis 42.5–47 cm long. Pistillate flowers sessile; ovary c. 1 × 1 cm, ± trilobed, densely

pubescent; styles 0.6–0.8 cm long, bright red, ± free at the base, laciniate. Fruits and seeds not seen.

Distribution. The exact country of origin is uncertain, but it is thought to be native to the Bismarck Archipelago and

Papua New Guinea (Radcliffe-Smith, 1996); it is widely cultivated elsewhere in Malesia, where it has also escaped into

surrounding forests (Sagun et al., 2010).

Occurrence in Singapore. This species appears to persist in abandoned areas as a remnant from former cultivation. It

was previously recorded by Chong et al. (2009) as “Cultivated Only”.

Local status. Casual; it is not known to set seed. This species is possibly dioecious as it is known only from cultivated

pistillate plants; there are no records of the staminate plants and perfect flowers, fruits and seeds (Sagun et al., 2010).

Plants are propagated exclusively from cuttings.

Specimens examined. SINGAPORE: Area near Thomson Nature Park, 29 January 2020, Chen, L.M.J., Lim, W.H., Athen,

P., Choo, L.M., Ho, B.C. et al., LCMJ 2020-057 (2 sheets) (SING).

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Fig. 1. Acalypha hispida Burm.f. from Chen et al. LCMJ 2020-057, collected from the area near Thomson Nature Park. (Photograph

by: W. H. Lim).

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2. Bixa orellana L. Sp. Pl. 1: 512 (1753) (Bixaceae)

(Fig. 2)

Key references. Yang & Gilbert (2007).

Description. Shrub to 2 m tall, younger branches densely reddish-brown-scaly. Leaves alternate; petioles 3.3–6.9 cm

long, ± covered with reddish-brown scales; lamina simple, broadly ovate, 10.5–19.3 × 5.5–9.9 cm, base truncate, tips

acute-acuminate. Inflorescence paniculate, flowers few to many; pedicels 0.5–0.6 cm long, covered with reddish-brown

scales; sepals and petals not seen; ovary ± ovoid, covered with soft prickles, c. 0.38 × 0.2 cm. Capsules drying dark brown,

covered with long prickles of 0.5–1 cm long, dehiscent when ripe, subglobose to ovoid, c. 2.2–4.3 cm long. Seeds

numerous, drying dark brown.

Distribution. Bixa orellana was domesticated by the native peoples in the Neotropics prior to the arrival of the Spanish

(Clement, 1999; Moreira et al., 2015). Its native range is thought to be in Amazonia, but the exact area may be obscure

because of the long history of cultivation. It is prized for the red-orange dye or ‘Annatto’ pigment which is extracted from

its seeds, and has naturalised in many parts of the tropics, including Hawaii (Imada, 2012), Puerto Rico (Liogier &

Martorell, 2000), Madagascar (Madagascar Catalogue, 2020) and West Africa (Catarino et al., 2008). Roxburgh recorded

the species as being present in India as early as 1832, but he had erroneously assumed it to be native to the country (de

Candolle, 1885).

Occurrence in Singapore. Bixa orellana was recorded earlier as naturalised in Singapore in the 1880s according to

Cantley (1883: A6), who included a list of plant species occurring as “undergrowth” in Singapore. However, Cantley

(1883) did not cite any specimens and provided no further details on its occurrence. It is perhaps not surprising that Bixa

orellana is not included as naturalised or casual in Chong et al. (2009), since government reports were not a usual “source

of literature” for reporting the occurrence of a naturalised plant species.

With Cantley’s account, we searched SING and located three specimens of Bixa orellana. Two of these were collected

by him, but did not have the exact dates or localities listed on the specimen labels. However, the pre-printed data on the

labels suggested that they were collected in Singapore in the 1880s. As there were no indications that the specimens were

collected from cultivated individuals, we think that these could be amongst the naturalised individuals mentioned by

Cantley (1883).

Even though specimens of Bixa orellana from Singapore were absent, there can still be no doubt about the high fecundity

of Bixa orellana and its ability to multiply and persist locally, at least during the 1880s. Ridley (1888) wrote that “...the

Arnotto reproduces itself very rapidly, and forms a low dense bush, under which nothing can grow,” and listed the

“Arnotto” or Bixa orellana as one of the trees that could outgrow and kill Lalang grass (Imperata cylindrica).

The most recent collection of Bixa orellana from a non-cultivated source was taken from along Mandai Road in 1948,

after which there were no more collections. It remains to be seen if this species will again naturalise in Singapore, as it is

still cultivated as an ornamental in local parks and gardens (Chen et al., 2015).

Local status. Formerly naturalising/casual in Singapore. However, there are no collections of this species from the wild

after 1948, and it is likely that it is no longer extant because of the nation’s rapid pace of urbanisation and intensive

management of green spaces.

Specimens examined. SINGAPORE: s. loc., s.d., Cantley, N. s.n. (SING); ibid., Cantley, N. s.n. (SING); Mandai Road,

14 September 1948, Sinclair, J. SFN24799 (SING).

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Fig. 2. One of the two specimens of Bixa orellana L. collected by Nathaniel Cantley [SING 0201099]. The pre-printed locality (“Flora

of Singapore”) and date (“188_”) points to the possibility that these could be from the naturalised plants of Bixa orellana that Cantley

had listed in his 1883 report. (Photograph by: L. M. J. Chen).

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3. Bryophyllum tubiflorum Harv. Fl. Cap. 2: 380 (1862) (Crassulaceae)

(Fig. 3)

Key references. Descoings (2003).

Synonyms. Kalanchoe delagoensis Eckl. & Zeyh, Enum. Pl. Afric. Austral. 305 (1837); Kalanchoe tubiflora (Harv.)

Raym.-Hamet, Beih. Bot. Centralbl., Abt. 2. 29 (1): 44 (1912).

Description. Terrestrial herb. Stems succulent, erect or occasionally decumbent, to about 30 cm in length, with shoots

from c. 5 cm tall already forming vivaparious plantlets from the leaf apices. Leaves opposite, sessile, ± terete, 1.6–2.8 cm

long, succulent, with a shallow groove running lengthwise along the centre of the adaxial side; leaf colour variable, dull

green, bluish green or greyish brown, mottled with dark green or greyish-brown spots and streaks; leaf apex with 3–9

teeth; teeth spathulate, each often bearing a single vivaparious plantlet. Flowers not seen.

For a full description of the flowers, please see Morales (2010) and the online factsheet from Weeds of Australia (2016)

(listed as Bryophyllum delagoense). This species is a ‘LSDP’ or long-short day plant (Cajlahjan et al., 1970), and thus

requires a series of long days followed by short days in order to trigger flowering. It does not flower locally as there is

little variation in day length in Singapore.

Distribution. Native to Toliara (Tuléar) province in Madagascar (Madagascar Catalogue, 2020). Naturalised in Australia

(Weeds of Australia, 2016; as Bryophyllum delagoense), China (Wang et al., 2016), Taiwan (Wu et al., 2010), and Hawaii

(Imada, 2012). In Europe, it has been recorded as being present in France, Netherlands, Portugal and Spain (EASIN,

2020).

Occurrence in Singapore. This species, and Bryophyllum × houghtonii (D.B.Ward) P.I.Forst., which we recorded in an

earlier paper (Chen et al., 2018b), have both had a long history of cultivation in Singapore. As these plants are tolerant of

highly xeric conditions, the escapes from cultivation can often be found growing in cracks and fissures in walls, or on

exposed concrete surfaces. Fig. 3B shows a large clump of adult plants that established themselves on the roof ledge of

an abandoned building in Chinatown during the early 1990s.

Local status. Casual; the spread of this species is limited by its inability to flower and set seed under Singapore’s

conditions.

Notes. The genus Bryophyllum is often included in the broadly circumscribed Kalanchoe, although the relationship

between these two genera has been a subject of vigorous debate. Molecular phylogenetic studies suggest that they form a

clade (Gehrig et al., 2001; Mort et al., 2001), but taxon sampling and the number of DNA markers used have to be

increased in order to better understand the relationships between the two genera. As the results of the debate are far from

conclusive, we adopt the view that these should be considered as distinct genera (Moran, 2009). The species in our current

discussion falls within Bryophyllum s. str., based on the pendulous flowers and the presence of vivaparious plantlets borne

on the leaf margins.

This widely cultivated species has been circulated in horticulture as Kalanchoe tubiflora (Harv.) Raym.-Hamet., but many

sources have adopted the name Kalanchoe delagoensis Eckl. & Zeyh. following Descoings’s (2003) synoptic treatment

of the genus. However, Figueiredo & Smith (2017) argued that the “descriptive statement” provided by Ecklon & Zeyher

(1837) in the protologue of Kalanchoe delagoensis cannot be considered a diagnosis to meet the requirements for a validly

published name (Turland et al., 2018: Art. 38). As such, it was proposed that the correct name would be Bryophyllum

tubiflorum Harv., which we have also adopted here following Figueiredo & Smith (2017).

Specimens examined. SINGAPORE: Tanglin Shopping Centre: at lower edge of pavement, 22 May 1998, Lai, J. & Ali

Ibrahim LJ 373 (SING); Jurong Island: growing on volcanic rock substrate (escape from cultivation), 9 January 2019,

Lua, H.K. LCMJ 2019-108 (SING).

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Fig. 3. Bryophyllum tubiflorum Harv. A, young plants; inset shows the adventitious plantlets forming at the leaf tips, from Lua LCMJ

2019-108. B, mature plant in cultivation, Singapore. C, a small colony of mature plants that have escaped cultivation, having established

themselves on the concrete ledge of an abandoned building in Chinatown during the early 1990s. (Photographs by: L. M. J. Chen [A,

B]; Ali Ibrahim [C]).

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4. Calotropis gigantea (L.) W.T.Aiton Hort. Kew. ed. 2, 2: 78 (1811) (Apocynaceae: Asclepiadoideae)

(Figs. 4, 5)

Key references. Kiew (2001).

Description. Shrub to 1.5 m tall, with milky white sap, white-floccose on all vegetative parts. Leaves opposite; petiole c.

0.5 cm, white-floccose, with scattered, simple hairs at the base of the petiole; lamina simple, elliptical obovate, 11.7–17.5

× 6.8–9.6 cm, base with scattered simple hairs, cordate, apex acute. Inflorescence an umbel-like cyme, bearing 25–30

flowers; peduncle 12–13 cm long. Flowers to c. 3 cm across; pedicels 2.7–3 cm long, white-floccose; corolla light-to-

dark mauve or greenish-white, reflexed, lobes 1.6 × 0.65–0.8 cm; corolline corona absent; staminal corona fused to the

gynostegium, lobes 5, “laterally compressed, S-shaped”, 1.05–1.1 cm long, base with a ± inflated revolute spur, apex with

a tubercle on each side. Follicles ± cymbiform, c. 5.7 cm long. Seeds not seen.

Distribution. Calotropis gigantea is native to Southern China (Sichuan, Yunnan, Guangdong, Guangxi Zhuang

Autonomous Region and Hainan); Pakistan, India, Bhutan, Nepal and Sri Lanka on the Indian subcontinent (USDA,

2020); and Thailand in Southeast Asia (Kiew, 2001). It has apparently naturalised in some parts of Malesia (Kiew, 2001),

and is now pantropical in its naturalised range, having been recorded from many countries in the Indian Ocean (Mauritius

and Seychelles), tropical Africa (Congo, Gabon, Kenya and Tanzania) (Jiofack Tafokou, 2010; Witt & Luke, 2017),

Australia (Queensland) (Weeds of Australia, 2016), South America (Guyana, Suriname and Venezuela) and the Caribbean

area (Cuba) (Krings et al., 2005).

Occurrence in Singapore. In Chong et al. (2009), this species is recorded as “Cultivated Only”. Calotropis gigantea is

grown as an ornamental (Chen et al., 2015), and also as a larval food plant for the plain tiger butterfly or Danaus

chrysippus chrysippus (Butterfly & Insect Group—Nature Society Singapore, 2014; ButterflyCircle, 2016).

Local status. Even though Calotropis gigantea has been in cultivation for some time, wild individuals of this species

were only discovered recently when a thriving population was found on the open slopes between Bartley and the new

Bidadari Woodleigh Hillside housing estates. We consider this species to have naturalised in view that Calotropis

gigantea has been observed to be able to reproduce and form self-sustaining populations in the Bidadari area. This is

based on the many seedlings and saplings (more than 30 individuals) that were found alongside the adult plants that were

growing wild on wasteland in the vicinity of the estate, in areas that were undergoing construction, and also in the green

verges where this species has been planted in high density. While there may be concerns that the population on the slopes

of Bidadari may be ephemeral, the large number of cultivated and self-seeded plants growing along the green verges

spanning the entire estate will also be a source of propagules for further invasions in the area and beyond. The slopes on

which the plants have established are also part of a new park in the Bidadari area, and the area may be preserved as the

Housing & Development Board (HDB) has mentioned that the wooded and rustic nature of Bidadari will be retained to

create a unique park experience for visitors (Channel News Asia, 2019).

Notes. Calotropis gigantea is known to prefer climates with a distinct dry period and littoral, sandy soils. Its successful

establishment in Singapore could be due to the increasing episodes of prolonged hot and dry periods that the island has

been experiencing in recent years, possibly in response to global warming.

Specimens examined. SINGAPORE: Bidadari Woodleigh Hillside, on slope facing new HDB estate, 13 January 2020,

Chen, L.M.J. LCMJ 2020-001 (2 sheets) (SING); ibid., 13 January 2020, Chen, L.M.J. LCMJ 2020-002 (SING); ibid.,

13 January 2020, Chen, L.M.J. LCMJ 2020-003 (SING); sapling in planting verge next to road, 13 January 2020, Chen,

L.M.J. LCMJ 2020-004 (SING); sapling on slope facing new HDB estate, 13 January 2020, Chen, L.M.J. LCMJ 2020-

005 (SING); sapling at edge of construction site, 13 January 2020, Chen, L.M.J. LCMJ 2020-006 (SING).

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Fig. 4. Calotropis gigantea (L.) W.T.Aiton, on slopes of Bidadari Woodleigh Hillside estate. A, mature plant (mauve-flowered form)

near the access routes to the park; B, flowers of mauve-flowered form; C, unripe follicle; D, plant of white-flowered form; E, flowers

of the white-flowered form. A–C from Chen LCMJ 2020-002; D–E from Chen LCMJ 2020-003. (Photographs by: L. M. J. Chen).

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Fig. 5. Calotropis gigantea (L.) W.T.Aiton in Bidadari Woodleigh Hillside estate. A, caterpillar of Danaus chrysippus chrysippus

(plain tiger), feeding on the leaves; B, one of many saplings along the slopes in the estate; C, sapling at construction site along Upper

Aljunied Road. A from Chen LCMJ 2020-003; B from Chen LCMJ 2020-006. (Photographs by: L. M. J. Chen).

ACKNOWLEDGEMENTS

We thank Ali Ibrahim for providing information pertaining to Bryophyllum tubiflorum Harv., and for allowing us to use

his photo for this publication. We also thank Derek Liew for his support in our field work.

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