Species Richness and Habitat Suitability of Myrmecophytes in Bengkulu : Host Tree, Coexist Epiphytes and Animals

Myrmecophytes or locally known as simbagh utak are common medicinal plants used by locals in Bengkulu, especially in South Bengkulu, for treating various diseases. Despite their potential as medicines, there is no report on biotic factors can be used to indicate of Myrmecophytes species’ richness and habitat suitability. The objectives of this research were to analyze the Myrmecophytes’ species richness and habitat suitability. This study used the purposive sampling method by exploring the area where Myrmecophytes were commonly found. The biotic factors of Myrmecophytes were analyzed by identifying the tree host, the other epiphyte plant grew around them, and animal occupants on the tuber of the Myrmecophytes. The Myrmecophytes distribution was analyzed by using ArcGIS10.1. The results showed that there were two species of Myrmecophytes, namely Hydnophytum formicarum and Myrmecodia tuberosa in the study area. The Myrmecophytes attached and hung in 9 species of host trees. The characteristics of host trees are high trees with large diameter, mostly rough-barked; some were cracked and mossy. The highest frequency of host trees included Hevea brasiliensis and Durio zibethinus. Myrmecophytes coexisted with 12 species of epiphytes. Epiphyte plants like Dendrobium sp. and Drymoglossum piloselloides can be used to indicate the presence of Myrmecophytes. Ants made up the most predominantly animal found living inside the tubers of Myrmecophytes, with some cockroaches and termites found at the tuber of Hydnophytum. Information on species’ richness and habitat suitability of Myrmecophytes can serve as supporting data for conservation efforts in Bengkulu to prevent the extinction of this species.

Because of the medicinal potential of Myrmecophytes, the factors affecting their existence on the environment need to be further investigated. Therefore, research on the species richness and habitat suitability of Myrmecophytes had been carried out. The purpose of this study is to identify the species and characteristics of the host trees, other epiphytes attached on the same host and the animals that inhabit the tubers of Myrmecophytes. Information on species' richness and habitat suitability of Myrmecophytes can serve as supporting data for conservation efforts in Bengkulu to prevent the extinction of this species.

Study area
The research was carried out from July 2015 to May 2016 in the Province of Bengkulu, Sumatera, Indonesia. Sampling was conducted in six districts in the Province of Bengkulu, namely South Bengkulu, Central Bengkulu, Bengkulu City, North Bengkulu, Seluma and Kaur ( Figure  1). The samples were identified in the Laboratory of Ecology and Plant Resources, Department of Biology, Faculty of Mathematic and Natural Sciences, Institut Pertanian Bogor, West Java, Indonesia.

Research procedure
The collection of Myrmecophytes was carried out using purposive sampling (Sutomo & Mukaromah 2010) in the six districts in the province of Bengkulu. Sampling for the initial data began with a survey of traditional markets and collection of Myrmecophytes information from the local residents.
As many as 51 plots (10x10 m²) were put on the Myrmecophytes collection spot. The sampling for other epiphytic species was carried out at a 3-6 m growth on the stems of host trees. All host trees, Myrmecophytes, other epiphytic plants on the same host, and animal occupants were collected as wet and dry specimens. The data recorded were collection number, location, date of collection, habitat, local name, morphological characteristics, utilization, and documentation. The plants' specimens were stored as herbarium specimens and identified at Laboratory of Ecology and Plant Resources, Department of Biology, Faculty of Mathematic and Natural Sciences, Institut Pertanian Bogor, West Java, Indonesia.

INTRODUCTION
The Myrmecophyte, used by the Indonesian people for traditional medicine, is one group of epiphytes plant that lives attached to a host tree. Myrmecophytes provide a nesting space for ants in their hollow plant parts. Myrmecophytes in Bengkulu province were known as Simbagh Utak. Simbagh means the plants attached to trees (epiphytes) and utak means brain. Epiphytic Myrmecophytes mainly belong to the Rubiaceae family, and only five genera of the group form bulbs, namely Anthorrhiza, Hydnophytum, Myrmecodia, Myrmephytum and Squamellaria (Huxley & Jebb, 1991). Some of these Myrmecophytes are traditionally used by local people in Indonesia to treat stomachache, cancer (Soekmanto et al., 2013;Senawong et al., 2013), tumors, coronary heart disease, hemorrhoids, tuberculosis, migraines, arthritis, leukemia (Khairudin et al., 2012), hepatitis, headache, diarrhea (Prachayasittikul et al., 2008), liver disease (Tatukude et al., 2014) and diabetes (Sianturi & Kurniawati, 2016). The application of the plants as medicines is performed by boiling the tuber and consuming the boiled water. Another way to use it requires putting pieces of the tuber in the sick body part.
The people of Bengkulu province collect these plants using a wooden pole that makes the young bud fall. This traditional collecting method will accelerate the extinction of this plant if left as it is without any conservation efforts. The conservation could be promoted by breeding the species, which requires Myrmecophyte materials such as seeds and samplings for cultivation (Sutomo & Mukaromah, 2010). However, the data for species cultivation of Myrmecophytes is still unavailable in the Province of Bengkulu, Indonesia.
Cultivation activities can be undertaken by utilizing the autecological data of Myrmecophytes. Autecology is the study of certain plant species in their natural habitat at an early stage effort in-situ conservation, and cultivation activities are an attempt of ex-situ conservation (Sutomo & Fardila, 2013). The parameters studied in autecology are abiotic and biotic factors of plants. The biotic factors of Myrmecophytes are the host tree, other epiphytes attached on the same host, and the animals that inhabit the tubers of Myrmecophytes. The factors biotic of Myrmecophytes can be used to indicate the species richness and habitat suitability of Myrmecophytes in Bengkulu Province. However, research on those species richness and habitat suitability of Myrmecophytes has never been undertaken in the province of Bengkulu. Data recorded on each plot of observation included the number of Myrmecophytes on a host tree, the height of growth in the host, the number of host trees, species of the host tree, the type of wood surface of the host and other species of epiphytic plants that coexist with Myrmecophytes.

RESULTS AND DISCUSSION
Myrmecophytes found in the Province of Bengkulu, Indonesia were Hydnophytum formicarum and Myrmecodia tuberosa. These plants were distributed in 5 districts out of 6 districts visited in Bengkulu Province, namely North Bengkulu, Central Bengkulu, Seluma, South Bengkulu, and Kaur. The distribution of H. formicarum is broader than of M. tuberosa. Hydnophytum formicarum were scattered in Kaur, Seluma, Central Bengkulu, to North Bengkulu whereas M. tuberosa were distributed in South Bengkulu and North Beng-kulu. M. tuberosa scattered in clusters in South Bengkulu district and H. formicarum was randomly distributed in four districts in Bengkulu Province (North Bengkulu, Central Bengkulu, Seluma, and Kaur). A previous study of Myrmecophytes occurrence based on their host tree in Bengkulu revealed that 77.8% of the plants spread randomly, and as many as 22.2% spread in groups (Safniyeti et al., 2017). The distribution pattern of Myrmecophytes is influenced by temperature and light intensity in the environment where they grow (Safniyeti et al., 2017).
Myrmecodia tuberosa found in Bengkulu has distinct morphological characteristics from H. formicarum. Myrmecodia tuberosa has thorns on the surface of its tubers and stems, clypeoli (a wing-shaped structure from the stem surface and considered as the protector of the stem), alveoli (pits on the stem surface where flowers and fruits emerged), pyrene (seed encapsulated by hardened endocarp) of 4-5, and narrow tuber cavities ( Figure 2). Hydnophytum formicarum has no spines on the surface of its tubers, stems, clypeoli, and alveoli. H. formicarum had flowers and fruits that were situated in the plant's leaf axilla, 1-2 pyrene in fruit, and its tuber cavities were larger than that of M. tuberosa (Figure 3).

Host tree of Myrmecophytes
Hydnophytum formicarum and Myrmecodia tuberosa found in Bengkulu were found attached to 9 host tree species (Table 1). Hydnophytum formicarum and Myrmecodia tuberosa grow individually or in groups on a host tree. Both genera Myrmecodia and Hydnophytum can be found on the same host tree and often occur together with several plants. Previous research reported the presence of epiphytic plants found only in certain tree species and on the part of certain trees (Febriliani et al., 2013).
Many of the host trees have rough barks (45.1%), while the rest of the trees (54.9%) have either mossy, cracked or slightly rough barks (Figure 4). Hevea brasiliensis, Durio sp., and Gmelina arborea are known to have a rather rough to very rough, mossy, uneven rods, slightly cracked bark texture (Febriliani et al., 2013) with many indentations (Sujalu et al., 2015) and holes (Sujalu 2007). Such trunk characteristics facilitate debris and dusts to accumulate on the tree, allowing the moisture build up on the tree surface (Sadili 2015). This tree surface serves as a conducive ground for the growth of Myrmecophytes and their seeds.
Durio sp. and H. brasiliensis were the host trees with the highest occupation frequency of the Myrmecophytes ( Figure 5). Most of the Myrmecophytes (47.06%) were found on H. brasiliensis at the height of between 5 m and 15 m, with the tree condition being at relatively low diameters ranging from 13.69-38.24 cm and at the free branch of tree 3-8 m. Durio sp. was the second most frequent host (23.53%) for the Myrmecophytes. Durio sp. found in this study has the largest diameter (95.54 cm) among all host trees. Gmelina arborea was the highest of all the host trees (23 m) and hosted 7.84% of the Myrmecophytes studied. Most of the Myrmecophytes (22 individuals) found in G. arborea grew at the height of up to 16 m. These results indicate that the Myrmecophytes favor to live higher up on a large-diameter tree (Sujalu et al., 2015), and these plants tend to like the host tree being homogeneous in one environment. Nevertheless, the Myrmecophytes also favor smaller trunk H. brasilliensis. Hevea brasiliensis is a crown-shaped tree with a height ranges from 5 to 15 m. At this height, the Myrmecophytes are able to get maximum sunlight. Gmelina arborea and Durio sp. have a dense canopy with a tree height ranging from 13 to 23 m and 3 to 16 m, respectively. In such canopies, the Myrmecophytes get enough sunlight, and at the same time still, allow the light to penetrate through and reach the surface of the Natural tourism forest (waterfall) Note: KT = Altitude grow; D = Diameter; BC = free branch of tree; TP = height of tree; Myr = Myrmecophytes; 0.00 = Not measured; HY = Hydnophytum formicarum ; MY = Myrmecodia tuberosa soil. Myrmecophytes require direct sunlight, as indicated by the way they grow. Myrmecophytes tend to stick and hang on the branches and stems (94%), as well as at the apex of the host tree's canopy (6%) (Figure 6). Myrmecophytes were also found to reside on the main stem of Delonix regia, at the height of 9 to 16 m. Despite growing up on the main stem of Delonix regia, the Myrmecophytes still receive maximum sunlight. This result is consistent with the results of PCA by Safniyeti et al. (2017) that shows the intensity of light is the main component of plant II, which affects the existence of Myrmecophytes.  In this present study, Myrmecophytes were found in the trees such as Archidendron jiringa, Artocarpus elasticus, Artocarpus integer, Durio sp., Delonix regia, Ficus racemosa, Gmelina arborea, Hevea brasiliensis, and Rhodamnia cinerea. Meanwhile, Parinding (2007) reported that Myrmecophytes grow on trees such as Melaleuca cajuputi, Melaleuca leucadendron, Melaleuca symphiocarpa and Acacia auriculiformis. Some Myrmecophytes also coexist with orchids. Both of these epiphytic plants utilize the host only as a place to adhere to (Febriliani et al., 2013). Furthermore, Parinding (2007) also reported that an ant nest could live on plants that have died. In addition to epiphytic plants, Artocarpus integer and Hevea brasiliensis trees can also be overgrown by parasitic plants (Kartika et al., 2016).

Other epiphytic plants coexist with Myrmecophytes
Other epiphytic species were found to coexist with Myrmecophytes, but that differed in each host species and also for each species of Myrmecophytes. We found as many as 16 individuals of the epiphytic plants in 51 host trees studied. Those epiphytic plants belong to 12 species ( Table 2). The most frequent epiphytic plants found are Simbagh pitis (Drymoglossum piloselloides) and Simbagh balung (Dendrobium sp.), which favor residing on Hevea brasiliensis, Artocarpus integer, Rhodamnia cinerea, Durio sp., and Archidendron jiringa trees. Interestingly, we found that both Drymoglossum piloselloides and Dendrobium sp., as well as Dischidia nummularia, coexisted with Hydnophytum and Myrmecodia, whereas the other epiphytic species exclusively coexisted with either one of the Myrmecophytes.
Asplenium nidus is only found in Myrmecophytes of the genus Hydnophytum (Table 2). Different epiphytic species found in each of the host trees could be due to environmental factors and the nature of each plant. For example, some epiphytic species have been found in trees that dwell in the shade and are not exposed to direct sunlight (Febriliani et al., 2013).
Dendrobium sp. and Drymoglossum piloselloides are the most prevalent epiphytes (21.43%) found in this study, and both coexisted with the two Myrmecophytes. Both of these plants are found in the roots and stems of the Myrmecophytes. Asplenium nidus was the next most predominantly found epiphytes with a frequency of 10.71% (Figure 7). In this study, we found that Asplenium nidus is coexisted only with Hydnophytum formicarum (Table 2) and grew at the bottom and the top of the Myrmecophyte. The fourth most frequent epiphyte plant was Dischidia nummularia. The plant was found to reside in the tubers of the two Hydnophytum formicarum and Myrmecodia tuberose. and branches that grow tightly, sheltered by tall trees and prefer the shade (<50%) (Puspitaningtyas, 2007). Epiphytic plants mostly dwell on branches or twigs that grow relatively flat or tilted (Sujalu et al., 2015); on a tree with stem diameter of > 20 cm. The most common branches dwelled by epiphytic plant is on the lower branch (Sujalu 2007) with thick bark shaded by a canopy (Mariyanti et al., 2015).

Animal occupants in the tuber of Myrmecophytes
The animals found in the tuber of Myrmecodia were typically ants with various sizes and colors, while the animals found in the tuber of Hydnophytum were termites, cockroaches, and ants (Table 3). Termites Macrotermes sp. found in the tubers of Hydnophytum that resided at the height of 54 m on Rhodamnia cinerea tree. The tuber of the Hydnophytum was moist and juicy with large tubers cavity (depth 3.5 cm). A cockroach Pycnoscelus sp. found in the tuber of Hydnophytum that were attached at the height of 133 m on the host Hevea brasiliensis tree. Ants living in the Myrmecophyte' cavity tubers consisted of several genera such as Crematogaster, Monomorium, Anoplolepis, Plagiolepis, and Philidris. These ants are usually found at an altitude of 25-629 m altitude and in a low-lying area. Previous research reported that Myrmecophytes are predominantly populated by the Iridomyrmex ant (Huxley, 1978), but the ant was not found in this present study. The altitude and natural habitat of Myrmecophytes affected the species that  Dendrobium sp., Agrostophyllum sp., Eria sp., Pholidota sp. and Flickingeria sp. were the orchid family (Orchidaceae) found at the study site. Previous research also reported that the Myrmecophytes and orchids coexist (Parinding 2007). These plants can coexist and do not interfere with each other, even though they reside in and utilize nutrients from the same niche.
Myrmecophytes and other epiphytic plants use tree species as their hosts, and their host preference depends on the climatic conditions of the forest stands (Febriliani et al., 2013), the crown density of the tree and host habitus (Puspitaningtyas, 2007). Epiphytic plants hide among twigs inhabit their tubers. Iridomyrmex is commonly found in Myrmecophytes which lives in savanna forests at an altitude of 0-1890 m altitude (Huxley & Jebb 1985).
Hydnophytum has a larger and deeper (± 2-7 cm) cavity compared to Myrmecodia, so the animals found within Hydnophytum tuber were of a diverse variety. Termites, cockroaches, wasps, centipedes, grasshoppers, lizards (Susanti 2016), geckos, frogs (Parinding 2007) and other invertebrates are animals found in the tubers of Hydnophytum, but not found in the tubers of Myrmecodia. Hydnophytum tubers found in this study were ± 1.5 cm in length, had cavities which were inhabited by ants (Figure 8). Meanwhile, Myrmecodia tubers were of a marble-size, hollow, and also inhabited by ants (Parinding 2007).
There were two species of ants, namely Plagiolepis pygmaea and Philidris sp. found inside the tuber of Hydnophytum. Whereas two different ant species, Monomorium destructor and Anoplolepis gracilipes were found in the tuber of Myrmecodia. The cavity and the depth of the Myrmecophytes tubers where those ants found are larger than those of the tubers where the termites were discovered ( Figure 9).  In this present study, Myrmecophytes found were Hydnophytum formicarum and Myrmecodia tuberosa. Both species is a medicinal plants used by locals in Bengkulu Province and most of which grew in the gardens belonging to the local community. The benefit of this research is to can be used as basic information to cultivation of Myrmecophytes, in addition the abundance of myrmecophytes is also used as a source of additional income for local people in Bengkulu Province.

CONCLUSIONS
In conclusion, Myrmecophyte species found in Bengkulu Province are Hydnophytum formicarum and Myrmecodia tuberosa. The Myrmecophytes attached and hung in 9 species of host trees, most of which grew in the gardens belonging to the local community of Bengkulu Province. Myrmecophytes coexisted with 12 species of epiphytes. Among the epiphytes, Drymoglossum piloselloides and Dendrobium sp. were found to be associated with both Myrmecophytes; thus, their presence can serve as an indicator for the occurrence of the two Myrmecophyte species. The animals found living inside the tuber of Myrmecodia were all ants, whereas the animals found in the tuber of Hydnophytum were largely ants with a very small number of cockroaches and termites.