Balanophora Papuana Schltr. (Balanophoraceae), a Neglected Holoparasite Species: Rediscovery for Indonesia

Damayanto IPGP, Riastiwi I. 2019 P.15 Balanophora papuana Schltr. (Balanophoraceae), a Neglected Holoparasite Species: Rediscovery for Indonesia

I Putu Gede P. Damayanto1, Indira Riastiwi

Herbarium Bogoriense, Botany Division, Research Center for Biology, Indonesian Institute of Sciences – LIPI Jl. Raya Jakarta-Bogor km 46, Cibinong, Bogor, West Java. 16911. Indonesia.

Abstract Balanophora papuana Schltr. is a parasite plant on a root of another plant, herbaceous, without chlorophyll and has attractive colours such as yellow to red. This species is distributed in northern and western part of Sumatra, Malay Peninsula, Borneo-Malaysia (Kinabalu), northern and western part of Sulawesi, Seram Island, Philippines (Luzon, Mindoro and Mindanao) and Papua New Guinea. Although reportedly spread throughout Indonesia, unfortunately, there is no collection of B. papuana in Herbarium Bogoriense (BO), Indonesia. However, based on GBIF data reported that there are several specimens of B. papuana collected in a period of 1928 to 1979 from Sumatra that stored in Herbarium at Leiden (L) but we have never seen that specimens. In northern Sumatra, Ridley in 1923 reported that found one species of Balanophora, but it could not be further identified due to the incomplete specimen. In 2012, research on Balanophora diversity was conducted in West Sumatra and yet did not found B. papuana. Recently, Research Center for Biology – LIPI was conducted a flora exploration to North Sumatra and found a complete specimen of B. papuana. It confirms the existence of B. papuana in North Sumatra after 39 years without any collection. Notes on this species were reported on this paper. Photographs of the fresh specimen are also provided.

Keywords: Balanophora papuana, rediscovery, North Sumatra, Indonesia

1. Introduction Indonesia has approximately 30,000‒40,000 species of Spermatophytes [1] including parasite plants. Parasite plants are often overlooked by botanists but others can be so well known such as Rafflesia spp. The life-way of Rafflesia spp. is unique because they take the nutrients from a root of another plant due to the absence of chlorophyll for photosynthesizing. Rafflesia spp. is considered rare as a result of its unique biological properties [2]. Another parasite plant such as Balanophoraceae is often neglected by botanists in Indonesia, although it is one of the parasite root plants that is also categorized as rare plant [3]. So far, there has been few research on Balanophoraceae in Indonesia, some of them were the monograph of Malesian Balanoporaceae [4], [5], the anatomy study of two species of Balanophora [6] , the anatomy study of vascular bundles in two species of Balanophora [7], the diversity of Balanophoraceae in West Sumatra [3] and the diversity of Balanophora spp. in Mt. Halimun Salak National Park [8]. On the other hand, Balanophoraceae-related research outside Indonesia has been largely done (see [9],

1 Corresponding author. Tel.: +62-21 8795066; fax: +62-21 8765059 E-mail address: [email protected].

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[10], [11], [12], [13], [14], [15], [16], [17], [18] and many others). Some of their research is the publication of the new species, diversity, flower development, anatomy and ultrastructure, pollination mechanisms and chemical content. According to Hansen [5], Balanophoraceae is parasite plants on a root, herbaceous plants without chlorophyll and has attractive colours such as whitish to yellow, brown, orange to red or pink. The stems appear from the tubers in an endogenous or exogenous manner. Balanophoraceae can either have leaves or not. Inflorescences in a spadix with unisexual flowers (male and female not in one plant) or bisexual (male and female in one plant). One of the Balanophoraceae species that reported grow in Indonesia is Balanophora papuana Schltr. [4], [5], [10]. Based on the distribution map from Hansen [5], B. papuana is reportedly distributed in northern and western Sumatra and Sulawesi, Seram Island, and widely distributed in Papua and West Papua also. While the distribution of B. papuana outside Indonesia is found in the Malay Peninsula, Borneo- Malaysia (Kinabalu), Philippines (Luzon, Mindoro and Mindanao) and New Guinea. Although reportedly spread throughout Indonesia, unfortunately, there is no collection of B. papuana in Herbarium Bogoriense (BO), Indonesia. However, based on GBIF data, there are several specimens of B. papuana that collected from Indonesia areas (Sumatra, Borneo, Sulawesi and Papua New Guinea) and stored in Herbarium at Leiden (L) and Kew (K) (see [25]). B. papuana was published as a new species from New Guinea by Schlechter in 1913 [10]. Although B. papuana is reported growing scattered in western Sumatra [5], research of Mukhti et al. [3] reported that no B. papuana found in West Sumatra. While in northern Sumatra, Ridley [19] reported found one species of Balanophora in this area but cannot be further identified due to the incomplete specimen. Previously, based on GBIF data, several specimens of B. papuana were reportedly collected from Sumatra [Aceh (Mt. Leuser), North Sumatra (Asahan, Mt. Sibayak and Tapanuli) and West Sumatra (Mt. Tandikat)] in period 1928 to 1979 that stored in Herbarium at Leiden (L) (see [25]). Unluckily, there is no photo of the specimens available in L. Recently, Research Center for Biology, Indonesian Institute of Sciences (LIPI) has been conducted the flora exploration to North Sumatra, around Toba Lake areas. One of the purposes of this study is to confirm the existence of B. papuana in North Sumatra and also get this species for herbarium specimen that stored in BO. The results of this study are presented in this paper.

2. Methods Flora exploration was conducted from 15 to 29 March 2018 using purposive random sampling method by Rugayah et al. [20] and located around Toba Lake areas, North Sumatra. Research sites were focused on forests in the north part of Toba Lake that have dense forest cover such as in Silalahi Forest, Silahisabungan District, Dairi Regency and Mt. Singgalang, Silimakuta District, Simalungun Regency. Fertile flora (with flower or fruit) was collected for deposited in Herbarium Bogoriense (BO). Some additional data

103 Damayanto IPGP, Riastiwi I. 2019 was noted such as location, altitude, GPS coordinate, habitat, date, vernacular name, utility, etc. Processing of the specimens at BO is following Djarwaningsih et al. [21], [22]. Identification of specimens is carried out by consulted with relevant reference i.e. [4], [5], [10] and based on digital herbarium specimens of Balanophora papuana that stored in worldwide herbaria or museum (if available) such as in Herbarium Royal Botanic Garden, Edinburgh (E), Herbarium Royal Botanic Gardens, Kew (K), Herbarium Rijksherbarium, Leiden (L), Museum National d’Histoire Naturelle, Paris (P), etc (see [23], [24]). Photographs of the fresh specimen are also be prepared.

3. Result and Discussion There are two collection numbers of Balanophora papuana specimens (Figure 1) that found from two different locations in the north part of Toba Lake. The first location near PLTA Lae Renun around Silalahi Forest, Silahisabungan District, Dairi Regency (02°47.168’N, 098°30.310’E) with an altitude 1580 m. The second location in Mt. Singgalang, near Nanggaraja Village, Silimakuta District, Simalungun Regency (02º57.311’N, 098º36.133’E) with an altitude 1552 m. The genus Balanophora comprises holoparasitic flowering plants that commonly parasitize the roots of a wide variety of plant species. The 15 recognized Balanophora species are distributed throughout temperate and tropical Asia, ranging at the eastern Australia to a western limit of Africa [4]. Species of Balanophora are having yellow, orange, or red inflorescences that emerge from warty tubers that are attached to their host plants [15]. The female flowers in Balanophora are comprised more than one million hair-like flowers estimated from a single inflorescence [4], while the male flowers are comprised of fused stamens that usually produce white pollen. Pollinators have been reported for a few species i.e. ants, cockroaches and moths [14]. Balanophora papuana was first described by Schlechter in 1913 based on two specimens of New Guinea, Schlechter 18250 from Finisterre Gebirges, 1300 m alt, collected on September 1908 (♂ plant) and Schlechter 18602 from Bismark, 1400 m alt, collected on November 1908 (♀ plant) [10]. Now, the first specimen is stored in P [26] and the last one is stored in P [27] and also K [28], [29]. He never mentioned the holotype of the specimens [see 10] and based on “Shenzhen Code”, both of that specimens are called syntype [see 30]. Syntype is two or more specimens that is listed in a description of a taxon where no holotype was designated in protologue [1], [31], where all specimens are equivalent. The absence of a holotype defined in protologue usually occurs before 1958 [33]. Actually, holotype is a single specimen designated as the basis for the description of a new species [32]. On the other hand, based on Tropicos data, the syntype specimen of B. papuana is from Irian Jaya (Indonesia): 15 km south west of Bernhard Camp, Idenburg River, open places between Pandanus prop-roots, an altitude 700 m, with collector Brass no. 12232, collected in January 1939 that stored at A (Herbarium, Arnold Arboretum of Harvard University) [34]. We think the data needs to be validated because no references are cited and Schlechter in 1913 [see 10] never mentioned this specimen on his protologue.

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Figure 1. Balanophora papuana Schltr. Remarks: A. Habit of pistillate plant (♀). B. Habit of staminate plant showing the flower (♂). C. Staminate plant from above (♂). D. Young staminate plant showing leaf arrangement (♂). Photos: I Putu Gede P. Damayanto from Damayanto & Rosalina 740 (BO)

Based on the specimen of Damayanto & Rosalina 740 (BO), the morphological characteristics of B. papuana as follows: dioeciously plant with red colour. Length from fusion with host root to top of inflorescences up to 13 cm. Tubers in a mass, diameter vary in size about 10‒20 cm, branching from the base. Stem with 4 pairs of opposite, decussate, obovate red leaves, which are patent during anthesis. The leaves are about

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3.5 by 2 cm. The leaves are always nearly of the same size, sometimes with 1 leaf smaller than the other. Male inflorescence 2‒5 by 1.5‒3 cm with expanded flowers. Flowers often in conspicuous vertical rows, bisymmetric or zygomorphic on account of lateral elongation. Synandrium with fertile part often slightly obconical, laterally elongated. Anther running from base to top of synandrium, longitudinally opening. Female inflorescence up to 1.5 by 2 cm and obovoid. Hansen [5] provides the illustrations of B. papuana as shown in Figure 2A‒B. Initially, we were in doubt with the existence of B. papuana with yellow colour. Previously, Hansen [5] mentioned that B. papuana has the yellow to orange-yellow or red colour. Furthermore, Deni Sahroni (staff of BO and also the collector of B. papuana), the person who told us that he ever has seen B. papuana with yellow colour in Kalimantan (Borneo), unfortunately, he did not collect that specimen and no photo was taken. Luckily, we found a photo of B. papuana (♂) with yellow colour (Figure 2C) on a database of the Tropicos [see 35]. That photo was taken from the collection of Callmander et al. no. 1204 (G, MO, SAN), located in Malaysia: Borneo, Ranau District, Mount Kinabalu Park, Mesilau (06°02’5”N, 116°35’52”E, 1900 m alt), collected on 14 October 2014 [35].

Figure 2. Balanophora papuana Schltr. Remarks: A. Habit of pistillate plant (♀). B. Habit of staminate plant (♂). C. Habit of staminate plant with yellow colour. Photos: A & B from [5], C from [35]

Species B. papuana grows in evergreen mountain forests at an altitude of 1000‒ 2000 m and rarely on 300‒1000 m [5]. Based on BO’s specimens, B. papuana grow in secondary forest at an altitude about 1500 m. Hosts of this species are recorded: Macaranga sp. (Euphorbiaceae) and Ficus sp. (Moraceae) [5]. There is no record of hosts plant of B. papuana on the BO’s collections. These species are reported flowering all the year round, 66% of dated collections from June to November [5]. In this research, this species found flowering in March.

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In 2010, Hosoya, et al. [17] successfully isolated the papuabalanols A (1) and papuabalanols B (2), two new dehydrohexahydroxydiphenoyl (DHHDP) esters of dihydrochalcone glycosides that obtained from the ethyl acetate extract of B. papuana. Furthermore, they tested that compounds in mice. They reported that papuabalanol A (1) caused moderate vasodilator effect on aorta of mice, while papuabalanol B (2) caused potent inhibition of mushroom tyrosinase and antimelanogenesis in B16 mice melanoma cells. Specimen examined: Indonesia: North Sumatra, Dairi Regency, Silahisabungan District, Silalahi Forest, near PLTA (hydroelectric power plant) Lae Renun, 02°47.168’N, 098°30.310’E, 1580 m alt, 26 March 2018, Damayanto & Rosalina 740 (spirit collection of ♂ and ♀) (BO); North Sumatra, Simalungun Regency, Silimakuta District (Saribu Dolok), Nanggaraja Village, Mt. Singgalang, 02º57.311’N, 098º36.133’E, 1552 m alt, 24 March 2018, Damayanto & Sahroni 544 (dry collection of ♀) (BO). Additional specimen examined: Philippines: the Island of Mindanao, District of Davao, Todaya (Mt. Apo), June 1909, Elmer 10870 (dry collection of E, digital specimen barcode E00313813; K, digital specimen barcode K000674587). New Guinea: Aud den Kämmen des Finisterre Gebirges, 1300 m alt, 8 September 1908, Schlechter 18250 (dry collection of ♂) (P, digital specimen barcode P06619694); Wälder des Bismark, 1400 m alt, 1 November 1908, Schlechter 18602 (dry collection of ♀) (K, digital specimen barcode K000674591; P, digital specimen barcode P06619693).

4. Conclusion Balanophora papuana was successfully rediscovered in Sumatra. There are two collection numbers of B. papuana specimens that found near PLTA (hydroelectric power plant) Lae Renun around Silalahi Forest and Mt. Singgalang in North Sumatera. It confirms the existence of B. papuana in North Sumatra.

5. Acknowledgements Dr Pieter B. Pelser (CANU) is gratefully acknowledged for the hospitality and suggestion during the identifying the specimen. Thanks go to Kusuma Rahmawati, S.Hut., Dewi Rosalina (BO), Agus Haryadi (BO) and Deni Sahroni (BO) for hospitality during the fieldwork. Abdulrokhman Kartonegoro M.Si. (BO, L) is gratefully acknowledged for his hospitality to help us finding the Balanophora Monograph in Leiden (L). Thanks go to herbaria of E, K, and P for the digital images of their specimens and also to Martin W. Callmander Ph.D. (Conservatoire et Jardin Botaniques de la Ville de Genѐve) and also other collectors: S. Buerki, C. Davidson, S. Christoph, P. Miun and J. Jumian for granted permit using their photograph of yellow Balanophora papuana. Sincerely thanks to Flora Malesiana Journal for their illustrations of B. papuana.

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[31]. Hansen HV, Seberg O. 1984. Paralektotipe, a new type term in botany. Taxon 1984;33(4):707-711. [32]. Ardiyani M, Dwibadra D, Dewi K, Mulyadi, Meliah S, Maryanto I, Rustiami H, Arifiani D, Rahajoe JS, Sutrisno H, Kanti A. Temuan dan pertelaan jenis baru biota Indonesia 1967-2017: sumbangsih LIPI untuk sains. Jakarta: LIPI Press;2017. [33]. Eggli U, Leuenberger BE. Type specimens of Cactaceae names in the Berlin Herbarium (B) (de Herbario Berolinensi notulae no. 48). Willdenowia 2008;38:213- 280. [34]. Tropicos. Balanophora papuana Schltr. [internet]. Missouri: Missouri Botanical Garden; 2018. Available from: http://www.tropicos.org/Name/50099191. [35]. Tropicos. Balanophora papuana Schltr. [internet]. Missouri: Missouri Botanical Garden; 2018. Available from: http://www.tropicos.org/Image/100349984.

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