WILD ORCHID DIVERSITY OF HIGHLAND FOREST IN THE HEART OF BORNEO: LONG BANGA AND TAMA ABU, SARAWAK

The Heart of Borneo (HoB) initiative facilitates conservation and environment protection while enhancing sustainable development that safeguards the welfare of natural resources and inhabitants of the island. The HoB research e�pedi� tions conducted in the Long Banga and Tama Abu were aimed to document the highland orchid species inhabited in one of the largest remaining transboundary rainforests in the world, which are racing dissolution from their habitat. Thus the resolution for their conservation in situ and ex situ could be drafted meritoriously. The research e�peditions in the protected transboundary forest areas revealed a total of 206 species and 59 genera. A total of 118 species of 46 genera were recorded during the HoB Long Banga 2016 e�pedition, while 117 species in 46 genera were found from the HoB Tama Abu 2017 e�pedition. Roughly 70% of the species documented were epiphytes. A few of them were mycoheterotrophs, such as Aphyllorchis pallida, Cystorchis aphylla, and Tropidia saprophytica, and several «jewel» orchids, including Cystorchis stenoglossa and Macodes petola. Astonishingly, we discovered a number of endemic and newly recorded orchid species for Borneo. In Long Banga, the riverine forests are home to a higher number of orchids than the inland forests, owing to the presence of host trees with a spreading crown structure and moist bark te�ture suited epiphyte colonisation. In addition, the riverine forests are banked by a swampy alluvial vegetation that encourage the terrestrial species to grow in. Sites of the inland forests were seen disturbed with wide canopy gaps lacking of the emergent layer. Contrarily, in Tama Abu, the inland forest perceived as the more preferable habitats for orchids to thrive in as it was an undisturbed forested belt. In addition, they had a higher humidity essential for the orchid growth. It was not surprisingly, that a high abundance of orchid species was encountered in the undisturbed inland hill forest roofed with dense tree canopy cover. The hills transitioned into a montane vegetation with a lower number of species. This parameter peaked in a mossy forest, a distinct habitat harbouring endemic and rare species. In addition, ten endemic species are assessed as EN B2b(iii). Herewith, our discovery infers the need for a continuous biodiversity monitoring and conservation assessment to maintain orchid species survival and to reveal the accurate species richness within the highland habitats of Sarawak. Additionally, underlined herein is the need for establishment of an arboretum or a conservation centre for orchids to accommodate the botanical study.


Introduction
Orchids belong to the family Orchidaceae and are considered to be the most fascinating and valu� able group of flowering plants advanced in the flo� ral variation and distinctive form among the mono� cotyledons (Go et al., 2010). Appro�imately, about 25 000-35 000 of orchid species with 800-1000 genera are distributed throughout the world (Go� goi et al., 2012). Malaysia is well�endowed with orchids. It is estimated that as abundant as 972 spe� cies occur in Peninsular Malaysia and 3000 spe� cies occur in Borneo (Lamb, 1991;Beaman et al., 2001;Ong et al., 2017). Orchids are adapting to different types of ecosystems, especially in tropi� cal mountainous regions and isolated islands (Has� sler & Rheinheimer, 2013). Some of them adapted to e�treme dry conditions such as the semi�desert habitat (Pridgeon, 2014).
Orchids are of conservation objectives due to their research and commercial importance, and in� trinsic aesthetic value within their habitats (Flores� Palacios & Valencia�Diaz, 2007;Cruz�Fernández et al., 2011). Unfortunately, orchids are also quite well� known among the endangered species. A large num� ber are neglected and may not have been discovered yet because of the loss of habitat resulting from hu� man activities in the Borneo region (Wood & Cribb, 1994;Edwards et al., 2012;Gaveau et al., 2014). Concentrated on the highland forest of Borneo is one of the world's greatest centres for orchid diversity that grows as epiphytes, terrestrials, mycoheterotrophs, lithophytes or rheophytes (Wood & Cribb, 1994;Beaman et al., 2001). Also, each mountain range has its own distinctive features that support a wealth of flora and fauna, including orchids (Wood & Cribb, 1994;Beaman et al., 2001;Majit et al., 2014). It is within the Heart of Borneo (HoB), which is part of the transboundary conservation initiative that spreads across Borneo central highlands forests of Malaysia, Brunei, and Indonesia. The HoB ambitious initiative covers an area of 26 900 km 2 spanning across si� ad� ministrative divisions and nine districts.
There are lacking records on orchids native to highland forests in Northern Borneo, as the last known data collected from the area was made 124 years ago (Ridley, 1896;Go & Pungga, 2018). This earliest enumeration of orchids in the northern part was procured by Ridley (1896) based on the collec� tions by Dr. Haviland and Bishop Hose in Sarawak and Mr. Pryer in Sabah, together with other enthusi� asts in Singapore. The most recently published botan� ical survey on orchids of Borneo was done about two years ago in Belaga (Ling & Sang, 2018), although the area is not a highland, but a low forested hill.
For these reasons, an aspiring conservation pro� gramme, «Sarawak Heart of Borneo» that covers not just any area in Borneo, but highland forests at the core or the «heart» of the island was initiated. It is aimed to identify and create an inventory of all orchid species that e�ist in the mountainous area before they become e�tinct along with their habitat, and to con� serve them in situ and ex situ. To date, a vast majority of diversity and ecological research were focused on the northern parts of Sarawak. However, uncontrolla� ble forest e�ploitation drove rapid deterioration to the forests of the region, and rescuing them is one of the main objectives of the HoB conservation programme. This paper is a first demonstration of the orchid diver� sity, with a focus on highland vegetation in the north� east part of Sarawak, in the Tama Abu range, and the inventory was done through the e�ploration (Fig. 1).
Also, reported here is our first assessment on the con� servation status of the endemic yet endangered orchid species in Borneo. An appraisal of flora biodiversity and their conservation status is an essential step to� wards the conservation of forest biodiversity.

Material and Methods
Botanical surveys were carried out in pristine hill to montane forest in the Long Banga and Tama Abu in the Tama Abu Range from 21 August 2016 to 1 September 2016 and from 13 August 2017 to 27 August 2017, respectively. Long Banga and Tama Abu are located in the Tama Abu range surrounded by Dayak's rural villages located in the northeast of Sarawak, Ulu Baram, in the Marudi division. The geomorphology of Tama Abu range with e�tension to the Kelabit Highlands in the northeast illustrates «backbone» highlands of Sarawak. However, de� backbone» highlands of Sarawak. However, de� » highlands of Sarawak. However, de� highlands of Sarawak. However, de� tailed geological information of this large forest area is deficient. We are deprived of an in-depth descrip� tion of soil and geomorphological features in the mentioned area. Though there are at least two rock formations similar to Meligan Formation and Kelabit Formation in Kelabit Highlands that probably e�ist in this area based on previous brief geological reports of Liechti et al. (1960), Haile (1962) and Thomson (2015). Also, referable, a description of the major vegetation types of Pulong Tau National Park was made by Pearce (2006). Therefore, in order to enrich the published information, our observations noted during the e�peditions are incorporated. Geographically, Long Banga and Tama Abu share comparatively similar vegetation types as in Bario highland and Pulong Tau, located in the Northeastern part of Sarawak, too (Beaman et al., 2001;Pearce, 2006). The Tama Abu Permanent Forest Reserve is located at the south�eastern part of Pulong Tau National Park, Ulu Baram, near the border with Indonesia. It is characterised mainly by over�logged forests and forests affected by shift� ing cultivation carried out by the indigenous peo� ple (Durst et al., 2005;Ling et al., 2019). Patches amidst inland forests are still in fairly good con� dition despite the past logging activities as shown by the emergence of many large trees (Ling et al., 2019). There is a highland plateau of over 1000 m a.s.l. The Long Banga and Tama Abu forests are comparable to Pulong Tau's, where the studied areas consist of mi�ed dipterocarp forest, alluvial and riverine, hill and lower montane vegetation types, e�cept lacking or absence of upper montane and kerangas or tropical heath forests. The lower moisture and temperature were strongly influenced by both altitude and the presence of forest canopy (Pearce, 2006). Also, its permanently wet and rich mineral soil in the riverine, alluvial and mossy forests filled with humid air encourage mosses to grow on the trees makes the trees and ground a fit� ting habitat for orchids to root in (Wood & Cribb, 1994;Pearce, 2006).
Specimens were processed according to the standard herbarium specimen preparation tech� niques outlined in Bridson & Forman (2000) and stored in the Sarawak Herbarium (SAR), Forest Research Centre, Sarawak, Malaysia. Living speci� mens were processed according to Go et al. (2015). Some living collections were also made and brought back to the Research, Development, and Innovation Division (RDID) in Sarawak Forestry Department for propagation in the nursery. Reliable references were used in the identification and classification processes, including published accounts of Wood (1997Wood ( , 2003, and Beaman et al. (2001). Currently accepted names of the orchids were checked using the KEW World Checklist of Selected Plant Fami� lies (WCSP) (Govaerts et al., 2020).
An assessment of the proposed conservation status was evaluated only for the endemic species. A guideline in IUCN Red List Categories and Crite� ria version 14 (August 2019) (IUCN Standards and Petitions Committee, 2019) was followed. The cur� rent information gathered on the endemic species are more applicable towards the assessment based on the geographical range in the form of the cur� rent E�tent of Occurrence (EOO) and Area of Oc� cupancy (AOO) of each species. The generalised information used in this study have been based on three main sources of information: (i) review of available literature, documents, and geo�referenced herbarium specimens; (ii) fieldwork in the accessi� ble forests in Peninsular Malaysia and Borneo; (iii) personal and professional e�perience, including in� ference, suspicion, projection, and e�pert consulta� tion. The range of distributions of each species was assessed using Geospatial Conservation Assessment Tool (GeoCAT) (http://geocat.kew.org/) (Bachman et al., 2011). The range of distribution from histori� cal and current localities within Borneo was plotted in Google Earth maps. GeoCAT was also used to estimate the E�tent of Occurrence (EOO) and Area of Occurrence (AOO) (Bachman et al., 2011). E�� tinction risk for each species was determined based on Criterion B (IUCN Standards and Petitions Com� mittee, 2019). The current conservation status was checked using the IUCN Red List of Threatened Species database (http://www.iucnredlist.org).

Species abundance and diversity
The research e�peditions accumulated a to� tal of 118 species and 46 genera from three trails and non�trails, and a total of 117 species and 46 genera were collected from nine pre�creat� ed trails and one non�trail in the hills to lower montane forest, in Long Banga and Tama Abu, respectively. In total, we collected 206 orchid species belonging to 59 genera from the two highland forests in the Tama Abu range. How� ever, 43 species of them were identified only at genus level due to the lack of floral structures or flowers alcohol collections. The living plants were cultivated in the RDID's nursery to induce flowering prior to further identification, but only a few of them were blooming. Consequently, the identification of the incomplete specimens was made based on the diagnostic morphology of vegetative structures alone. The results of the two research e�peditions are listed in Electronic Supplement 1 (see Fig. S1, Fig. S2, Fig. S3, Fig.  S4) and Electronic Supplement 2.
The composition of orchid genera found in Tama Abu was very similar to data obtained in Long Banga, where Bulbophyllum, Dendrobium, and Coelogyne were the most abundant genera collected. The remaining genera were Agrostophyllum, Appendicula, Liparis, Oberonia, Phalaenopsis, Pinalia, Phaius, and Vanda (Fig. 2). The discovery of several Phalaenopsis species and a Vanda species in the Tama Abu forest astonished us, because these genera are recorded with a small distribution range and low occurrence in both Bor� neo and Peninsular Malaysia region.

Species abundance based on subfamilies and growth habits
The species composition is represented most� ly by the Epidendroideae subfamily (198 species, 96.12%) and the remaining subfamilies are Aposta� sioideae (two species, 0.97%), Orchidoideae (five species, 2.43%) and Vanilloideae (one species, 0.49%), where this also reflects the high richness of epiphytes (176 species, 85.44%) found during the e�peditions in these two habitats. The remain� ing 23 species (11.17%) were found as terrestrial plants, including five species of mycoheterotrophs (2.43%) that obtain nutrients from mycorrhizal fungi (Fig. 3).

Species abundance and diversity based on vegetation types
In Long Banga, our field collection had yielded us with 63 orchid species from the riv� erine forests (Fig. 4). The inland area was more disturbed and gaps were apparent. The species diversity can be considered as high given the possibility that the area may have been over� logged. More orchids were found in the riverine forest compared to the inland montane forests in Long Banga owing to the less disturbed canopy and ground conditions. It is also assumed dur� ing the sample collection that in the riverine area these orchids were easily collected by hands, without the need for tools or to climb trees. Prob� ably because of this, many epiphytic species were usually collected and documented (Ling & Sang, 2018). However, here we make another conclusion on it. In the riverine forest, the mois� ture level was equally ideal as in a primary inland forest as it was constantly moisturised by the flowing stream. The height of the riverine trees, where the orchids grew on, were of average size. Despite of that, the orchids were still in a high abundance. The deep shade provided by wide branching of the riverine trees has made the envi� ronment favourable for the moisture�lover plants, such as mosses and shade�loving orchids to grow in (O'Malley, 2009;Benítez et al., 2015). Like� wise, the trees with widely spreading branches would equally have also e�posed the sun�loving epiphytic orchids to the sunlight (Timsina et al., 2016). On these sites, the tree crowns are dense and banked by alluvial vegetation with a shallow peat layer which may never e�perience soil water deficits (Pearce, 2006). In addition, there was no evidence that in the riverine forest, the orchids are being negatively affected by flood, which im� plies a better chance of survival and pollination.  Although the orchids were less abundant, the inland forest was still harbouring a great diversity of orchid species. It may probably be caused by the presence of large and varied types of host plants for epiphyte colonisation. It could be e�pected that shade�demanding species of Bulbophyllum, Dendrobium and Coelogyne would be in the highest abun� dance in canopy�protected forests with less direct e�posure to the sun rays as favourable (Ling & Sang, 2018;Besi et al., 2019b). These groups are mostly composed of highland orchid species with coria� ceous or leathery leaves, with or without pseudob� ulbs, and adapted only to wet and cool conditions (Seidenfaden & Wood, 1992;Wood et al., 1993;Besi et al., 2019b). Still, some vegetation patches were opened with wide canopy gaps. These canopy gaps may be caused by natural disturbance, including windfall, lightning strike, and death of an emergent individual trees from a pathogen (Ashton, 2008). In addition, it could be due to many pioneer and succes� sional plant species, which increased in abundance following past logging in the area (Newman, 1990;Demies et al., 2019). However, our claim appears predictive, inferred from empirical observation dur� ing the e�ploration, though as yet we have no sup� porting evidence. Without the canopy protection, full sunlight and radiation reach and heat up the ground, altering the atmosphere and soil microclimatic strati� fications (Werner & Gradstein, 2009;Benίtez et al., 2015;Besi et al., 2019b). Even slight differences in the humidity may be considerable for fragile plants that highly dependent on water and organic matters for survivability (Werner & Gradstein, 2009). In ad� dition, we predict that in the hill forest, the reduc� tion of the continuous suitable habitat poses a seri� ous ecological conundrum causing a remarkably low abundance of the orchid community.
In Tama Abu, on the contrary, a high abundance, and diversity of orchid species was harvested from the inland hills and montane forests with dense tree canopy and relatively undisturbed ground, including the terrestrial and mycoheterotroph orchids (Fig. 4). The constantly wet environment was not just affect� ing the ground condition, but also had promoted the growth of mosses on the trees and rocks. This reflects the high number of epiphytes encountered during e�� peditions (Wood et al., 1993;Wood & Cribb, 1994;Benítez et al., 2015). The e�tensive stands of mature and large trees form an emergent layer with inter� locked canopy that provide the shaded and well�wa� tered sites for the terrestrial orchids. One more factor is the thick humus layer covering the moist ground, which certainly provides the nourishment to the ter� restrial orchids, and the mycoheterotroph orchids re� lying on mycoheterotrophy at some point in their life cycle, especially at germination (Leake, 1994;Leake et al., 2004;Leake & Cameron, 2010). These plants are inconspicuous and have an ephemeral lifestyle hidden from a plain sight. Their mycorrhizal symbi� osis with both fungal partners and autotrophic plants depends much on the soil stratification (Martos et al., 2009;Leake & Cameron, 2010). In addition, the lower montane mossy forest is an important habitat specialised with a specific vegetation structure and is relatively continuous. This specialised habitat is characterised by a high orchid endemism.
The riverine forest was populated by trees with small trunks and branches with layered and thicker crown rather than spreading. It makes them less favourable for epiphytes to grow on. Small trunks and branches reduce space for colonisation for epiphytic plants. In tropical forests, the distri� bution and abundance of epiphytic species depend on the different host characteristics (Hietz, 1999;Callaway et al., 2002;Partomihardjo et al., 2004;Adhikari et al., 2012;Hsu et al., 2014).

Rareness and endemism of orchids
A known commercially important orchid ta�on, Vanilla, is a genus that contributes to the Vanilla flavour in our daily foods (Raffi et al., 2017). Vanilla from Borneo is understudied due to a low number of collections from the field and infrequent flowering (Cribb, 2014;Ling & Ong, 2016). Until now, only five species are recorded for Sarawak (Ling & Ong, 2016). Vanilla was also found along with the terrestrial and «jewel» orchids, including Cystorchis javanica (Blume) Blume, Cystorchis stenoglossa Schltr., Cystorchis variegata Blume, and Macodes petola (Blume) Lindl. (Fig. S1). The rarely encountered myco� heterotroph orchids were equally found in Long Banga and Tama Abu, such as Aphyllorchis and Cystorchis (Fig. S1). An e�ception is three rarely encountered orchid species Bromheadia rupestris Ridl., Dendrobium tetrachromum Rchb.f., and Nephelaphyllum tenuiflorum Blume, found only in Tama Abu (Fig. S1).
Furthermore, we highlighted here the discovery of ten endemics, yet endangered orchid species in Borneo, including Calanthe crenulata J.J.Sm.  (Fig. S2).

Conservation assessment of the endemic species
In Borneo, Orchidaceae is one of the top pri� ority rescue families listed in the Wildlife Protec� tion Ordinance, 1998(Laws of Sarawak, 1998. However, there is no publication that could spe� cifically pilot orchid conservation assessment neither in Borneo nor in Sarawak. About 10% of the discovered orchid species, including endem� ics (Fig. 5), have a restricted distribution area. However, we found a group of incompletely identified species (20%), which could harbour a higher number of endemic and rare species. The narrowly distributed and highland-confined spe� cies require large stands of forest for reproductive success. Now, these are facing e�tinction due to the loss of vital pollinators and genetic erosion (Cribb et al., 2003;Memmott et al., 2007). Thus, conservation of the specialised habitats with dis� tinct floras, especially those rich in endemics, should then aim to legislate (Ashton, 2008).
Hence, we include our first result on the proposed conservation status assessment for the ten endemic species of Borneo found in Long Banga and Tama Abu, including data on their current distribution, AOO, and EOO val� ues (Table). GeoCAT maps show their current e�tent of occurrence (Fig. 6).
Based on the current IUCN Red List of Threatened Species, only Tropidia saprophytica has been globally assessed for its conser� vation status. It is classified as Least Concern (Chadburn, 2014). This orchid species is rarely seen and easily unnoticed in the wild (Wood et al., 1993;Chan et al., 1994) because it is in� conspicuous, and on the basis of its small size it has a brownish but light�coloured appearance that resembles the leaf litter and often secluded under the understory vegetation. This orchid was recorded in Protected Areas in Sarawak, Sabah and Brunei. However, such areas may still be e�posed to anthropogenic and naturo� genic disturbances (Chadburn, 2014). Our fur� ther survey on the population status, ecology and specific threats affecting T. saprophytica in the Tama Abu forest shows that now it is more correct to the threatened IUCN category rather than as Least Concern.
On the basis of the estimation of their pro� posed conservation status, we assessed the en� demic species as Endangered ta�a, EN B2b(iii) ( Table), with estimated AOO is less than 500 km 2 and continuing decline in e�tent and qual� ity of habitat (IUCN Standards and Petitions Committee, 2019). The estimated EOOs e�� ceed the thresholds needed for the threatened IUCN category, and the current collection lo� cations are still situated within Protected Areas for some of these endemic species. However, all species occur within narrow AOOs in Bor� neo, in the hills and lower montane forests. In Borneo, the mentioned forest types are now facing rampant anthropogenic destructions, mainly logging for timber e�traction (Wood et al., 1993;Ashton, 2008). Below we discuss the foreseen anthropogenic threats occurring around the forest margins in Long Banga and Tama Abu. Due to the rampant tree e�traction activities, their at�risk habitats are qualified them as one of the most threatened. Also, in re� gard to the most vulnerable mycoheterotrophs orchids, their lacking of chlorophyll and nor� mally developed leaves entails its high depend� ence on the ground or soil conditions (Leake & Cameron, 2010;Campbell, 2014). In addition, it is not known to be conserved ex situ. In any case, this would be very difficult because of its dependence on soil fungi (Campbell, 2014;Chadburn, 2014).
The habitat reduction positively influences the species e�tinction rates. The removal of the forest fragments and host plants cause rapid population decline of the inhabitants (Grad� stein, 2008). The habitat destruction may have gradually driven many orchid species close to e�tinction (Mondragon & Calvo�Irabien, 2006). It is debatable whether assisted geographical and marginal migrations can overcome the dis� turbance even with the presence of their adap� tive survival strategies in accordance with the environmental alterations caused by climate changes (Cribb et al., 2003).    . 6) may probably underestimate due to the e�clusion of doubtful specimens depos� ited in the local herbaria and specimens with in� sufficient data on the locality. The qualitative data will undoubtedly adjust upon further identification of specimens. Nonetheless, the system remains fairly adjustable to ensure that ta�a, of which with very limited information is known, could also be assessed. To estimate the continuing decline in habitat area for B2b according to IUCN criteria, we incorporated inferences, suspicions, and pro� jections to test a ta�on. This was highly based on an empirical study carried out by the authors and on evaluation of attached notes on the available herbarium specimens. We cannot ignore the im� portance of these inferences, suspicions, and pro� jections. Here, the partial but continuous biodiver� sity monitoring is useful and must be documented (IUCN Standards and Petitions Committee, 2019). For the endemic species found in Long Banga and Tama Abu areas, the proposed conservation status could provide information for the IUCN Red List categories and criteria assessments.

Notes on records of orchids new to Borneo
There are no comprehensive records published on orchids in the Tama Abu range. To date, minor data are available on the diversity of wild orchids in the surrounding areas represented by similar vegetation structures to Long Banga and Tama Abu forests and considerably the nearest ones: (i) the earliest record of orchids in Borneo first coined in Ridley (1896); (ii) a checklist of the orchids in Borneo including Kalimantan and Brunei (Wood & Cribb, 1994); (iii) a checklist of flora, fauna, food and medicinal plants in the Lanjak Entimau Wild� life Sanctuary (Chai, 2000); (iv) records of orchids in the Kelabit highlands (Beaman et al., 2001); (v) a record on the flora of Pulong Tau National Park (Pearce, 2006); (vi) Orchidaceae diversity in Mu� rum Dam, Belaga, Sarawak (Ling & Sang, 2018). Until now, the mentioned records and checklists are of most reliable accounts to evaluate the abun� dance and distribution of each species collected in Northern Sarawak. Below we present the new or� chid records, including brief information on their habit, locality, habitat, current distribution status, and specimens e�amined.

Conclusions
The generalised records obtained from the two e�peditions in the northeast region of Sarawak's Heart of Borneo strengthens the idea that the Sarawak's highland forest harbours a vast variety of orchid species. A total of 206 species and 59 genera were collected from the inland montane and riverine forests, as well as non�trail sites in Long Banga and Tama Abu forests. Bulbophyllum, Dendrobium, and Coelogyne were the genera with the highest number of species. Most of the documented species were epiphytes, including ten endemics and threatened species, as well as two species newly recorded for Borneo. Here, we emphasise the importance and influence of each vegetation type on the species abundance, where the highest diversity was found in the inland montane forests. In the inland montane forests, undisturbed sites were dominated by emer� gent trees with dense and spreading crown structure providing moisture that is suitable for both epiphyte and terrestrial plant colonisation. However, an even higher diversity of orchids could be e�pected, if all found specimens were fertile. Therefore, further cultivation of the living plants in an arboretum or an ex situ conservation prior to species identification is undoubtedly important.

Supporting Information
Photographs of selected orchid species known in Tama Abu and Long Banga, Heart of Borneo (Electronic Supplement 1: Orchid species found in Tama Abu and Long Banga, Sarawak, Heart of Borneo), and a detailed distribution of orchids in the study area (Electronic Supplement 2: List of orchid species found in the highland forests in Long Banga and Tama Abu, Heart of Borneo, including information on the growth habits and localities) may be found in the Supporting Infor� mation here.