Philippine Journal of Science 150 (S1): 151-163, Special Issue on ISSN 0031 - 7683 Date Received: 21 Sep 2020

Richness and Distribution of Orchids () in the Forests of Mount Busa, Sarangani, Southern Mindanao,

Aljohn Jay L. Saavedra1,2 and Kier Mitchel E. Pitogo2

1Philippine Taxonomic Initiative, Inc. El Nido, Palawan 5313 Philippines 2Department of Environment and Natural Resources Provincial Environment and Natural Resources Office South Cotabato Block 1, Martinez Subdivision, Koronadal City 9506 Philippines

Orchids are one of the most diverse yet threatened families in the world and the Philippines. Despite the new discoveries of orchids in the country in recent years, diversity and distribution studies are still severely lacking. Here, we provide a list of orchid species found among different forest types in Mount Busa and provide information on the species’ altitudinal and vertical distributions and ornamental use. We recorded 108 species of orchids from 51 genera, of which 53 species are endemic to the Philippines and 15 species are known only to occur on Mindanao island. Species composition differed among forest types, with the MASLEF (mixed advanced secondary lowland evergreen forest) hosting the highest number of orchid species recorded, followed by the UMF (upper montane forest), LMF (lower montane forest), and MESLEF (mixed early secondary lowland evergreen forest). Our results suggest a relatively rich and distinct orchid diversity among different forest types in Mount Busa that reinforces the high conservation value of the mountain range.

Keywords: Mindanao biodiversity, serrulata, orchid conservation, orchid distribution, orchid inventory, Philippine orchids

INTRODUCTION orchids are the most threatened group of globally (Gale et al. 2018) and in the Philippines (Fernando et Orchids are one of the largest and most diverse groups al. 2008a). It is estimated that 56.5% of the 948 orchid among the Philippine flowering plants harboring over species assessed in the Global IUCN Red List in 2017 1200 species, varieties, and forms (Cootes 2011), with are threatened with extinction (Gale et al. 2018). In more new species and genera being discovered and the Philippines, 97 species are already threatened that recorded yearly (e.g. de Leon et al. 2017; Naive and represents ~ 8.1% of the orchid species recorded in the Martyr 2018; Meneses and Cootes 2019; Naive et al. country (DENR 2017). 2019; Tamayo et al. 2020; Tandang et al. 2020). This group of plants is mostly habitat specialists owing to Habitat destruction and unsustainable harvesting are the their specialized reproductive strategies and mycorrhizal major global threats to orchids (Fay 2018; Gale et al. 2018). specificity (Gravendeel et al. 2004). Unfortunately, Habitat fragmentation negatively impacts species richness of orchids (Hundera et al. 2013; Parra Sánchez et al. 2016), *Corresponding Authors: [email protected]

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and their highly specialized habit makes orchids more ecology and addresses the gaps in our knowledge and vulnerable to global environmental changes (Fay 2018). distribution of Philippine orchids. Our results would be Orchids are also highly traded mainly for , helpful not only in elucidating the level of biodiversity in medicine, and food (Hinsley et al. 2017). Despite being southern Mindanao but also in inferring patterns of plant regulated under the Convention on International Trade in diversity and biogeography in the Philippines. Endangered Species, many of the species are still being collected and traded undocumented negatively affecting wild populations around the world (Fay 2015). MATERIALS AND METHODS The increasing pressure on wild orchid populations put orchids as a group of urgent conservation concern. Despite the new orchid species discoveries in recent years, Study Area diversity and distribution studies are still severely lacking We surveyed orchid species richness along the southern (Buenavista 2017; Betanio and Buenavista 2018). This gap slope of Mount Busa, Kiamba Municipality, Sarangani may pose conservation challenges for this highly threatened Province between July 2019 and August 2020. Mount plant family, as assemblage-level studies may serve as Busa, known as “Bulul Tembob” among the local Tboli, baselines for future monitoring programs in Philippine is located at N 06°06.537’ E 124°41.026’ and reaches montane ecosystems, particularly for the highly collected 2046 m in elevation, which makes it the highest point in and traded orchids. Distribution studies also help inform Sarangani. It houses one of the last remaining primary species conservation assessments (e.g. IUCN Red List forests in southern Mindanao. On 10 Mar 2020, the of Threatened Species and Philippine Red List), as these Provincial Government of Sarangani formally declared provide information on the species’ extent of occurrence the southern slope of Mount Busa a local conservation and geographic range. area by resolution 2020-10-042. One of the major mountains in southern Mindanao with Mount Busa was stratified into forest types based on the relatively intact lowland and montane forests is Mount classification of Fernando and colleagues (2008b). We Busa. It is a key biodiversity area (KBA) and one of the further classified the lowland evergreen forest into two: extremely high conservation priority sites in the Philippines the forest ranging in elevation from 400–600 m is the (Ong et al. 2002). Portions of Mount Busa may have formed MESLEF and the forest from 700–1100 m elevation is the part of the older landmass of the Zamboanga Peninsula– MASLEF. The lower elevation of Mount Busa (400–1000 Daguma Range block, which collided with the more recent m) was hardly hit during the logging concession in the central and eastern Mindanao blocks in the Middle Miocene, early 1990s, hence the dominance of secondary-growth thus forming the present-day Mindanao island (Sajona et trees at this elevation (see Brown 2015). al. 1997; Hall 2002; Yumul et al. 2004). The accreted The forest from 1200–1600 m elevation is the LMF and Mindanao island was intermittently connected directly to from 1700–2046 m elevation is the UMF (Figure 1). Five and the rest of the Sundaland through land bridges sampling points with more than 200-m distance in between due to repeated sea-level oscillations during the Pleistocene were randomly chosen in each forest type to maximize the glacial cycle (Brown et al. 2013). These events may have diversity of other habitat types surveyed, although we did shaped the present-day patterns of diversity in southern not limit our search to pre-defined plots. Habitats surveyed Mindanao, which necessitates more field-based biodiversity include agricultural plots of abaca, riparian areas, moist studies in Mount Busa. This is relevant for orchids, as the ravines, grasslands, shrublands, litter, and forest trails. diversity of some orchid genera in the Philippines were shaped by this complex geological history (Guo et al. 2015; Tsai et al. 2015, 2020). In addition, biodiversity studies in Field Sampling southern Mindanao remain scanty, especially for orchids in Opportunistic sampling was done in each sampling site by the region that do not have empirical field data yet available four to five experienced individuals, which entailed careful in published literature. and extensive examinations of understory and midstory layers of the forest for ground and epiphytic orchids. This Here, we provide an inventory of orchid species found in was done with the caveat that orchid species beyond 4 m Mount Busa with information on altitudinal and vertical above the ground might have not been recorded due to distributions and their ornamental uses. Since orchid inaccessibility or observer bias. Encountered fallen trees distribution is influenced by elevation and species’ traits and branches, however, were thoroughly searched for (Jacquemyn et al. 2005; Zhang et al. 2015; Ding et al. 2016), canopy-dwelling orchids. we also examined the pattern of orchid species richness among different forest types in the area. This information The altitudinal range and vertical distribution were noted helps improve our understanding of orchid diversity and for each orchid species observed in the wild. The altitude

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Figure 1. A contour map of the southern slope of Mount Busa, Sarangani Province showing the sampling sites in different forest types. MESLEF – mixed early secondary lowland evergreen forest, MASLEF – mixed advanced secondary lowland evergreen forest, LMF – lower montane forest, UMF – upper montane forest. was recorded using a Global Positioning System (Garmin et al. 2020), and the species’ conservation status was 64sc, USA), and the height at which the orchid was based on the DAO 2017-11 of the Philippine Department observed (vertical distribution) was visually estimated of Environment and Natural Resources (DENR 2017). using the height of AJS as reference. Only flowering The Philippine Department of Environment and Natural orchid species were included in the list. We also surveyed Resources (DENR) issued the fieldwork and collection houses in four villages, locally called as “sitios,” around permit for this study (Gratuitous Permit No. 2020-09). the vicinity of Mount Busa (Tulad, Datal Bong, Banate, and Green Valley) to check for orchids collected by the Statistical Analysis local people for ornamental use that we missed in the wild. We examined sampling adequacy using sample-size- All orchid species encountered were photographed in situ based and coverage-based rarefaction and extrapolation whenever possible. We did not collect voucher specimens for (R/E) curves and a sample completeness curve for species conservation reasons. Only one or a few individuals of most richness (data type= incidence; Chao1). These were species of orchids recorded were observed, and many of these computed and plotted with 95% confidence intervals species are already being collected for ornamental use. All in the R package iNEXT (Hsieh et al. 2016). A similar species were identified based on photographic guides (Cootes analysis was used to check for orchid species richness 2001, 2011; Pelser et al. 2011 onwards), expert consultations among forest types in Mount Busa. The R/E curves allow (e.g. through the online plant identification platform of the us to evaluate sampling completeness and facilitate a Co’s Digital Flora of the Philippines; Barcelona et al. 2013), conservative comparison of species richness among the and taxonomic papers in orchids (Clements and Cootes 2009; forest types despite the differences in the sampling effort. Cabactulan et al. 2018). Only those species observed in the wild were included in the analysis. We performed the analysis in the R statistical We also checked the distribution of each identified species software Version 1.1.463 (R Core Team 2020). using the aforementioned resources. Nomenclature follows the World Checklist of Orchidaceae (Govaerts

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RESULTS ornamental plants by the local people, 11 species were not observed in the wild. Only five species are threatened We recorded 108 species of orchids from 51 genera under the DAO 2017-11, one of which is listed as (Table 1), at least four of which were putatively new critically endangered (Grammatophyllum wallisii), three and undescribed species – namely, Bulbophyllum sp. 3, as endangered (Phalaenopsis sanderiana, Phalaenopsis sp., sp., and sp. 2. reichenbachiana, Renanthera monachica), and one as The sampling completeness curve shows that almost 50% vulnerable (Phalaenopsis mariae). coverage was attained for all sites (Figure 2B), suggesting that additional fieldwork would still increase the species We report range extensions of at least nine species which richness of orchids, as shown in extrapolated curves are also new island records for Mindanao – namely, (Figures 2A and 2C). Thrixspermum elmeri, which was previously recorded in Negros; Cylindrolobus longissimus, Erythrodes latifolia, The most speciose genera were (11.1%), Rhomboda lanceolata, Blepharoglossum grossum, and (9.3%), and Bulbophyllum (6.5%). Fifty- Odontochilus marivelensis in Luzon; Dendrobium boosii in three (53) species are endemic to the Philippines, of Luzon, Mindoro, Negros, and Leyte; loheri which 15 species are known only to occur in mainland in Cebu, Luzon, and Samar; and Paraphaius flavus in Luzon, Mindanao. Of the 32 orchid species that were utilized as

Table 1. Initial list of orchid species in Mount Busa, Sarangani, Philippines. Altitudinal distribution Vertical Local Endemism No. Species Distributionc (masl)a distribution useb 1 mantinianum L.Linden & Cogn. 550 Ground Orn. Yes Philippines 2 Acriopsis liliifolia var. lilifolia (J.Koenig) Seidenf. 400–500 4 m – No Widespread 3 Agrostophyllum elongatum (Ridl.) Schuit. 500 1.5–4 m – No Widespread 4 Agrostophyllum loheri Ormerod 600–700 2.5 m Orn. Yes Philippines 5 Anoectochilus sp. 800–900 Ground – – – 6 Appendicula crotalina (Ames) Schltr. 500–600 2–5 m Orn. Yes Mindanao 7 Appendicula elmeri (Ames) Ames 800 2 m – Yes Mindanao 8 Appendicula leytensis Ames house – Orn. Yes Sam-Ley 9 Appendicula malindangensis (Ames) Schltr. 1800–2000 1.5–4 m – Yes Philippines 10 Appendicula cf. pendula Blume 800–900 1.7 m – No Widespread 11 Appendicula undulata var. longicalcarata 650-900 2 m Orn. No Widespread (Rolfe) Ames 12 Appendicula weberi Ames 1150 1.6 m – Yes Philippines 13 Appendicula sp. 1 600–700 1.5 m – – – 14 Appendicula sp. 2 600–700 1.5 m – – – 15 Appendicula sp. 3 800 3–6 m – – – 16 Appendicula sp. 4 800 2 m – – – 17 Appendicula sp. 5 1500–1600 1.5 m – – – 18 Blepharoglossum condylobulbon (Rchb.f.) L.Li 800 2.5 m – No Widespread 19 Blepharoglossum grossum (Rchb.f.) L.Li 1600–1800 4 m – No Luzon 20 unguiculata (Lindl.) Kocyan & Schuit. 800 2 m Orn. No Widespread 21 Bryobium senile (Ames) Schuit. 1600 0.3 m – Yes Philippines 22 Bulbophyllum antenniferum (Lindl.) Rchb.f. 650 2.5 m Orn. No Widespread 23 Bulbophyllum colubrimodum Ames 1370 2 m – Yes Philippines 24 Bulbophyllum mucronatum subsp. alagense (Ames) 1400–1600 1.5 m – Nod Philippines J.J.Verm. & P.O’Byrne 25 Bulbophyllum odoratum (Blume) Lindl. 600–700 2 m – No Widespread 26 Bulbophyllum sp. 1 1600–1700 1.7 m – – – 27 Bulbophyllum sp. 2 Sect. Stachysanthes 1300–1400 1.5–2 m – – – 28 Bulbophyllum sp. 3 Sect. Polymeres 1700–1800 5–10 m – – – 29 Calanthe davaensis Ames 1600–1800 Ground – Yes Mindanao

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Altitudinal distribution Vertical Local Endemism No. Species Distributionc (masl)a distribution useb 30 Calanthe cf. furcata Bateman ex. Lindl. 450 Ground Orn. Yes Philippines 31 Calanthe sp. “cf. kinabaluensis” 1500–1600 Ground – – – 32 aff.halconensis (Ames) S.S.Ying 1700–2000 Ground – Yes Philippines 33 Cheirostylis octodactyla Ames 2040 Ground – No Widespread 34 Coelogyne rochussenii de Vriese 400–700 Lithophyte – No Widespread 2 m 35 Coelogyne sp. 600–900 2–6 m Orn. – – 36 Corymborkis veratrifolia (Reinw.) Blume 400 Ground – No Widespread 37 Cryptostylis acutata J.J.Sm. 1400–1500 Ground – No Widespread 38 Cryptostylis taiwaniana Masam. 700–800 Ground – No Widespread 39 Cylindrolobus longissimus (Ames & Quisumb.) House – Orn. Yes Luzon J.J.Wood 40 Cymboglossum cymbidiifolium (Ridl.) Ormerod & 800–1000 2 m – No Widespread Cootes 41 Cystorchis sp. 550 Ground – – – 42 Dendrobium boosii Cootes & W.Suarez 700–1000 2–3 m Orn. Yes Philippines 43 Dendrobium cf. chloranthum Schuit. & Peter House – Orn. Yes Luzon B.Adams 44 Dendrobium orbilobulatum Fessel & Lückel 1100 4–5 m Orn. Yes Philippines 45 Dendrobium planum J.J.Sm. 500–600 5 m – Yes Philippines 46 Dendrobium plicatile Lindl. 1200 1.8 m – No Widespread 47 Dendrobium pterocarpum Ames 1800 7 m – Yes Mindanao 48 Dendrobium rhombeum Lindl. 700–1000 10–15 m Orn. Yes Philippines 49 Dendrobium setigerum Ames ex. M.A.Clem 850 10 m – Yes Philippines 50 Dendrobium tiongii Cootes 600–800 2–10 m Orn. Yes Philippines 51 Dendrobium uniflorum Griff. 500–600 2 m Orn. No Widespread 52 Dendrochilum coccineum H.A.Pedersen & Gravend. 1700–1800 1.5 m Orn. Yes Mindanao 53 Dendrochilum aff.elmeri Ames 1900–2000 1.5–3 m – Yes Mindanao 54 Lindl. 800 1.6 m – No Widespread 55 Dendrochilum migueldavidii Cootes & Cabactulan 900–1300 1.5–2 m – Yes Mindanao 56 Dendrochilum sp. 1 2000 2 m – – – 57 Dendrochilum sp. 2 800 1.7 m – – – 58 carinata Rchb.f. 1950 Ground – No Widespread 59 Epiblastus merrillii L.O.Williams 1150 3.5 m – Yes Mindanao 60 Epipogium roseum (D.Don) Lindl. 600–700 Ground – Yes Philippines 61 Erythrodes latifolia Blume 700 Ground – Yes Luzon 62 Grammatophyllum wallisii Rchb.f. 400–600 15–20 m Orn. Yes Philippines 63 Lepidogyne longifolia (Blume) Blume 1100-1200 Ground Orn. No Widespread 64 Mycaranthes candoonensis (Ames) Cootes & 1800–2000 2–5 m – Yes Mindanao W.Suarez 65 Mycaranthes mindanaensis (Ames) Cootes & 1600–1800 2–5 m – Yes Philippines W.Suarez 66 Oberonia serrulata Schltr. 500–700 2 m Orn. No Widespread 67 Octarrhena elmeri (Ames) Ames 550–650 2 m – Yes Mindanao 68 Odontochilus marivelensis Ormerod & Cootes 1600–1700 Ground – Yes Philippines 69 Odontochilus yakushimensis (Yamam.) T.Yukawa 2000 2.5 m – No Widespread 70 Oxystophyllum elmeri (Ames) M.A.Clem 800–900 3 m – Yes Philippines 71 Paraphaius flavus (Blume) J.W.Zhai, Z.J.Liu & 1700–1800 Ground – Yes Philippines F.W.Xing

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Altitudinal distribution Vertical Local Endemism No. Species Distributionc (masl)a distribution useb 72 Peristylus goodyeroides (D.Don.) Lindl. 700–900 Ground – No Widespread 73 tankervilleae (Bank) Blume 600 0.3 m – No Widespread 74 Phalaenopsis mariae Burb.ex R.Warner & House – Orn. Yes Philippines H.Williams 75 Phalaenopsis reichenbachiana Rchb.f. & Sander 450 4.5 m – Yes Mindanao 76 Phalaenopsis sanderiana Rchb.f. House – Orn. Yes Mindanao 77 imbricata Lindl. 400–600 4 m Orn. No Widespread 78 amesii Kraenzl. 1700 1.5 m – No Widespread 79 Phreatia sulcata (Blume) J.J.Sm. 1800 1.5 m Orn. No Widespread 80 Phreatia sp. 1 1700 1 m – – – 81 Phreatia sp. 2 1800–1900 1.5 m – – – 82 Pinalia floribunda(Lindl.) Kuntze 700–1500 1.5–3 m – No Widespread 83 Pinalia nielsenii 1900 1.7 m – Yes Mindanao Cootes, Cabactulan, & M.Leon 84 Podochilus lucescens Blume House – Orn. No Widespread 85 Podochilus plumosus Ames 1000–1100 2–3 m – Yes Philippines 86 Podochilus sp. 1000–1100 2–3 m – – – 87 Pteroceras longicalcareum (Ames & Rolfe) Garay House – Orn. Yes Philippines 88 Renanthera monachica Ames House – Orn. Yes Philippines 89 Rhomboda lanceolata (Lindl.) Ormerod 1800–2000 0–2 m – No Widespread 90 Robiquetia bifidus(Lindl.) Kocyan & Schuit. House – Orn. Yes Philippines 91 Robiquetia compressa (Lindl.) Schltr. 1400–1600 4 m – Yes Philippines 92 plicata Blume 400–1000 Ground Orn. No Widespread 93 cf. compressa (Blume) J.J.Wood 2000 1.5 m – No Widespread 94 Stichorkis gracilis (Ames) Naive & Ormerod 1600–1700 1.5 m – Yes Philippines 95 Stichorkis leytensis (Ames) Cootes 800–900 2.5 m – Yes Philippines 96 Stichorkis philippinensis (Ames) Naive & Ormerod 1500 1.7 m – Yes Philippines 97 Taeniophyllum philippinense Rchb.f. 2000 1.7 m – Yes Philippines 98 Taeniophyllum sp. 580 1.9 m – – – 99 carinata Blume 500–1300 1.5 m – No Widespread 100 Thrixspermum bellamabantae Cabactulan, Cootes & 480 2.5 m – Yes Mindanao R.B.Pimentel 101 Thrixspermum elmeri L.O.Williams 1950 2 m – Yes Negros 102 Thrixspermum merguense (Hook.f.) Kuntze 500 2–2.5 m – No Widespread 103 Thrixspermum rostratum Ames 500 2.5 m Orn. Yes Philippines 104 Thrixspermum sp. 600–700 3 m – No – 105 Trichotosia odorifera (Leav.) Kraenzl. House – Orn. Yes Philippines 106 Trichotosia aff.ramosii (Leav.) Kraenzl. 1500–1700 15–20 m – Yes Philippines 107 Vanda cootesii Motes House – Orn. Yes Mindanao 108 Vrydagzynea sp. 1650–1725 Ground – No – aSpecies that were solely recorded in the villages were denoted as house bOrn. – species used as ornamental plants cWidespread – species that are native but not endemic in the Philippines; Philippines – Philippine endemic species that were found in two or more major islands; Luzon – endemic species that were recorded only in Luzon island; Negros – endemic species that were recorded only in Negros island; Sam-Ley – endemic species that were recorded only in Samar and Leyte islands; Mindanao – endemic species that are known only to occur in mainland Mindanao. dThe subspecies is the Philippine endemic

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Mindoro, and Panay. We also recorded Oberonia serrulata, and 1100 m, although we expect an increase in species which is a new locality record for the species and the first richness in LMF and UMF (+ 1100 m elevation) with record for the Philippines (previously known to be endemic in subsequent fieldwork. Several plants we observed in the ; confirmed by Ronny Boos and Daniel Geiger). montane forests did not have or were past the flowering stage, making species identification difficult Most species of orchids were found in the MASLEF (700– or impossible (e.g. species in the genera Ceratostylis, 1100 m elevation) with 39 recorded species, followed by , Cylindrolobus, Dendrobium, Trichoglottis, the UMF (1700–2046 m elevation), LMF (1200–1600 Vanda). Thus, we recommend that fieldwork should cover m elevation), and MESLEF (400–600 m elevation) with the flowering seasons of various genera to maximize the 28, 20, and 17 recorded species, respectively (Figure 2). species inventory. On the other hand, MESLEF had the Orchids showed distinct species composition among lowest number of orchid species recorded, but this estimate forest types, as most species were narrowly distributed. may increase with the addition of new sampling areas. Only four species occurred in more than two forest The larger area in MASLEF, and the associated environmental types – namely, Dendrochilum migueldavidii, Pinalia variables that are optimum for many species to survive, could floribunda, Spathoglottis plicata, and . explain the high species richness estimate in this forest The lowland evergreen forest (MESLEF and MASLEF) type (species-area relationships in mountains; McCain was mostly composed of species under the genera and Grytness 2010). Our results, although inconclusive at Appendicula, Dendrobium, and Thrixspermum (each present, suggest a mid-peak in species richness which is had more than two species in this forest type); commonly reported in the literature (Acharya et al. 2011; the LMF was dominated mainly by Bulbophyllum (four Salas-Morales and Meave 2012; Zhang et al. 2015; Betanio species) and Calanthe (two species but quite common and Buenavista 2018). However, the elevation at which the along forest trails in LMF); and the UMF by the genera diversity peaks differs across regions. Orchid diversity in Dendrochilum, Phreatia, Mycaranthes, Stichorkis, and the mountains in peak between an elevation of 1300 Appendicula (only A. malindangensis was found in UMF and 1800 m (Acharya et al. 2011; Zhang et al. 2015; Ding but it was the most abundant). et al. 2016) while mountains in tropical areas peak between 400 and 1000 m (Jacquemyn et al. 2005; Salas-Morales and Meave 2012; this study). In the Philippines, the forest between 400 and 1000 m elevation is mostly the tropical DISCUSSION lowland evergreen, which is the typical formation The biodiversity of southern Mindanao has long been in the country (Fernando et al. 2008b). underrepresented in the scientific literature, as evinced Species composition also differed among forest types, by the lack of published studies on biodiversity in the which may be due to certain traits that allow the species to region. Our study augments this gap and highlights the persist at certain elevations (Jacquemyn et al. 2005). This substantial level of biodiversity in southern Mindanao, distribution pattern suggests the distinctiveness of each particularly of the orchidaceous species which are among forest type in terms of orchid composition highlighting the most diverse yet threatened groups of plants globally the importance of encompassing all forest types in and in the Philippines. management interventions, as threats differ in kind and Mount Busa hosts ~ 9% of the country’s estimated number degree across elevation. For instance, the low-elevation of orchid species and harbors 53+ Philippine endemic forests are hardly hit by habitat degradation (Soh et al. species. This estimate is higher than other surveyed 2019) and montane organisms at all elevations are affected montane localities in the Philippines, with twice the by climatic changes as shown in the upward migration of number of recorded species in previous studies (18–60 mountain plants, causing range contractions of narrowly species; Panal et al. 2015; Buenavista 2017; Betanio and distributed species (Pauli et al. 1996; Lenoir et al. 2008; Buenavista 2018). It is even at par with the well-surveyed Bentley et al. 2019). Samar island that has at least 90 recorded orchid species Habitat degradation and climatic changes are exacerbated (Meneses et al. 2018). However, we acknowledge that by the poaching and harvesting of orchid species, which differences in species richness estimates could be due to remain a global threat to orchid populations (Fay 2018; observer bias and differences in the sampling coverage Gale et al. 2018). Local collections have been observed in and effort. Nevertheless, our results foreshadow the high the villages around Mount Busa for ornamental purposes, diversity of orchids in southern Mindanao, which is but we found no evidence yet of trade with outside plant worthy of conservation attention and further study. hobbyists and collectors. However, steps to regulate We recorded the highest orchid species richness in the collection from the wild should be undertaken because all MASLEF of Mount Busa between an elevation of 700 identified threatened orchids species in Mount Busa have

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Figure 2. (A) Sample-size-based and (C) coverage-based rarefaction (solid line) and extrapolation (dotted line) curves for species richness with 95% confidence intervals (shaded areas) for the orchid species recorded in Mount Busa. The solid triangle represents the reference samples. (B) Sample completeness curve linking curves in (A) and (C). The curves denote that additional field samplings would still yield more species.

Figure 3. Sample-size-based rarefaction (solid line) and extrapolation (dotted line) curves for species richness with 95% confidence intervals (shaded areas) for the orchid species recorded among different forest types in Mount Busa. The solid shapes represent the reference samples. LMF – lower montane forest, MASLEF – mixed advanced secondary lowland evergreen forest, MESLEF – mixed early secondary lowland evergreen forest, UMF – upper montane forest. been collected for ornamental use, three of which were diverse orchids in Mount Busa, particularly in the highly solely observed in the villages (e.g. Phalaenopsis mariae, diverse lowland evergreen forest where access is easier. Phalaenopsis sanderiana, and Renanthera monachica). It is Species that are range-restricted, endemic, and threatened for this reason why, as a precaution, we opted not to collect are likewise become vulnerable to poaching. species for voucher specimens since it might contribute to the reduction of orchid populations in the wild. Based on Our findings reinforce the Busa Mountain Range as a KBA our experiences, some locals have the tendency to collect and a high conservation priority site in the Philippines (Ong any plants that are identified as orchids, so we tried to be et al. 2002). The southern slope of the Busa Mountain discreet in documenting any orchid species. If poachers Range, where our study sites are situated, has been recently can penetrate the area then this could threaten the many declared as a local conservation area. Our findings and those

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Figure 4. Some of the orchid species recorded in Mount Busa: (A) Acanthophippium mantinianum; (B) Agrostophyllum elongatum; (C) Agrostophyllum loheri; (D) Anoectochilus sp.; (E) Appendicula crotalina; (F) Appendicula elmeri; (G) Appendicula leytensis; (H) Appendicula malindangensis; (I) Appendicula cf. pendula; (J) Appendicula undulata var. longicalcarata; (K) Appendicula weberi; (L) Appendicula sp. 1; (M) Appendicula sp. 2; (N) Appendicula sp. 3; (O) Appendicula sp. 4; (P) Appendicula sp. 5 (Q) Bryobium senile; (R) Bulbophyllum colubrimodum; (S) Bulbophyllum sp. 1; (T) Bulbophyllum sp. 2; (U) Bulbophyllum sp. 3; (V) Calanthe davaensis; (W) Calanthe sp. “cf. kinabaluensis”; (X) Cephalantheropsis aff. halconensis; (Y) Cheirostylis octodactyla.

of other studies (Brown 2015; Pitogo 2020) justify this legal southern Mindanao by providing an initial list of orchids protection, but a designation as a protected area under the in Mount Busa, noting certain ecological traits (i.e. NIPAS (National Integrated Protected Areas System) may altitudinal and vertical distributions) that are relevant be required to instigate more conservation and scientific to their conservation and to future studies on orchid attention given the high level of diversity, endemism, and ecology. We recommend more distribution studies undescribed species in the area. Many of the KBAs in the of orchids in the Philippines, particularly in montane Philippines remain unprotected (Mallari et al. 2016), which localities, since the data are needed in many conservation makes these areas vulnerable to illegal and unsustainable interventions (e.g. monitoring, conservation planning, activities. Empirical field data offer strong evidence to and species conservation assessments) and help infer justify protection and facilitate systematic conservation phytogeographical patterns in the country. Ecological planning (Margules and Pressey 2000). Field-based covariates that influence orchid distribution along biodiversity studies are particularly relevant in southern environmental gradients should be also explored because Mindanao, where threats of land conversion, mining, and this information remains scarce for Philippine species. illegal wildlife trade are becoming rampant. The difficulty of identifying orchid species could hinder such studies, but the availability of an online platform that This study provides a step towards strengthening the could connect early-career researchers (ECRs) and experts protection of one of the last remaining intact forests in

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Figure 5. Some of the orchid species recorded in Mount Busa: (A) Coelogyne rochussenii; (B) Coelogyne sp.; (C) Cryptostylis acutata; (D) Cymboglossum cymbidiifolium; (E) Cystorchis sp.; (F) Dendrobium boosii; (G) Dendrobium cf. chloranthum; (H) Dendrobium orbilobulatum; (I) Dendrobium plicatile; (J) Dendrobium pterocarpum; (K) Dendrobium rhombeum; (L) Dendrobium setigerum; (M) Dendrobium tiongii; (N) Dendrochilum coccineum; (O) Dendrochilum migueldavidii; (P) Dendrochilum sp. 1; (Q) Dendrochilum aff. elmeri; (R) Dendrochilum sp. 2; (S) Dienia carinata; (T) Epiblastus merilii; (U) Epipogium roseum; (V) Blepharoglossum grossum; (W) Mycaranthes candoonensis; (X) Mycaranthes mindanaensis; (Y) Oberonia serrulata. in the field help ameliorate this challenge (see Barcelona and Dan Sulan for their significant contributions to data et al. 2013). With enough technical support to ECRs, we collection. Tristan Luap Senarillos assisted us in the may be able to address many long-overdue questions in literature review and John Carlo Redeña Santos created the Philippine orchidology. map we used in this paper. We appreciate Rene Alfred Anton Bustamante, Wally Suarez, Ronny Boos, Daniel Geiger, Jim Cootes, and the many people in the Co’s Digital Flora of the Philippines Facebook page (and the platform itself) ACKNOWLEDGMENTS for helping us in the identification. Lastly, we thank the two anonymous reviewers who have helped in improving the We recorded the orchid species listed here in the course of early version of this manuscript. the Amphibians and Reptiles of Mount Busa project with financial support from The Rufford Foundation (Project No. 26752-1), USAID Protect Wildlife, and Idea Wild to KMP. DENR Region XII provided the permit for fieldwork REFERENCES (Gratuitous Permit No. 2020-09). We are immensely grateful to Lorenzo Sinandon, tribal chieftain of the Tulad ACHARYA KP, VETAAS OR, BIRKS HJB. 2011. Or- village, for sheltering us and ensuring our safety while chid species richness along Himalayan elevational on the field. We thank Nestor Gayan, John Timbangan, gradients. Journal of Biogeography 38(9): 1821–1833.

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Figure 6. Some of the orchid species recorded in Mount Busa: (A) Octarrhena elmeri; (B) Odontochilus marivelensis; (C) Phalaenopsis mariae; (D) Phalaenopsis reichenbachiana; (E) Phalaenopsis sanderiana; (F) Phreatia sp. 1; (G) Phreatia sp. 2; (H) Podochilus plumosus; (I) Podochilus sp.; (J) Renanthera monachica; (K) Rhomboda lanceolata; (L) Robiquetia bifidus; (M) Stichorkis cf. compressa; (N) Stichorkis gracilis; (O) Stichorkis philippinensis; (P) Taeniophyllum philippinense; (Q) Taeniophyllum sp.; (R) Thelasis carinata; (S) Thrixspermum elmeri; (T) Thrixspermum merguense; (U) Thrixspermum rostratum; (V) Thrixspermum sp.; (W) Trichotosia aff. ramosii; (X) Vanda cootesii; (Y) Vrydagzynea sp.

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