Aljohn Jay L. Saavedra 1,2 and Kier Mitchel E. Pitogo 2 1 Philippine Taxonomic Initiative, Inc. El Nido, Palawan 5313 Philippines 2 Department of Environment and Natural Resources Provincial Environment and Natural Resources Office South Cotabato Block 1, Martinez Subdivision, Koronadal City 9506 Philippines Richness and Distribution of Orchids (Orchidaceae) in the Forests of Mount Busa, Sarangani, Southern Mindanao, Philippines Keywords: Mindanao biodiversity, Oberonia serrulata, orchid conservation, orchid distribution, orchid inventory, Philippine orchids Orchids are one of the most diverse yet threatened plant families in the world and the Philippines. Despite the new species 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. *Corresponding Authors: [email protected]INTRODUCTION Orchids are one of the largest and most diverse groups among the Philippine flowering plants harboring over 1200 species, varieties, and forms (Cootes 2011), with more new species and genera being discovered and recorded yearly (e.g. de Leon et al. 2017; Naive and Martyr 2018; Meneses and Cootes 2019; Naive et al. 2019; Tamayo et al. 2020; Tandang et al. 2020). This group of plants is mostly habitat specialists owing to their specialized reproductive strategies and mycorrhizal specificity (Gravendeel et al. 2004). Unfortunately, orchids are the most threatened group of plants globally (Gale et al. 2018) and in the Philippines (Fernando et al. 2008a). It is estimated that 56.5% of the 948 orchid species assessed in the Global IUCN Red List in 2017 are threatened with extinction (Gale et al. 2018). In the Philippines, 97 species are already threatened that represents ~ 8.1% of the orchid species recorded in the country (DENR 2017). Habitat destruction and unsustainable harvesting are the major global threats to orchids (Fay 2018; Gale et al. 2018). Habitat fragmentation negatively impacts species richness of orchids (Hundera et al. 2013; Parra Sánchez et al. 2016), 151 Philippine Journal of Science 150 (S1): 151-163, Special Issue on Biodiversity ISSN 0031 - 7683 Date Received: 21 Sep 2020
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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
Richness and Distribution of Orchids (Orchidaceae) in the Forests of Mount Busa, Sarangani,
Orchids are one of the most diverse yet threatened plant families in the world and the Philippines. Despite the new species 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.
INTRODUCTIONOrchids are one of the largest and most diverse groups among the Philippine flowering plants harboring over 1200 species, varieties, and forms (Cootes 2011), with more new species and genera being discovered and recorded yearly (e.g. de Leon et al. 2017; Naive and Martyr 2018; Meneses and Cootes 2019; Naive et al. 2019; Tamayo et al. 2020; Tandang et al. 2020). This group of plants is mostly habitat specialists owing to their specialized reproductive strategies and mycorrhizal specificity (Gravendeel et al. 2004). Unfortunately,
orchids are the most threatened group of plants globally (Gale et al. 2018) and in the Philippines (Fernando et al. 2008a). It is estimated that 56.5% of the 948 orchid species assessed in the Global IUCN Red List in 2017 are threatened with extinction (Gale et al. 2018). In the Philippines, 97 species are already threatened that represents ~ 8.1% of the orchid species recorded in the country (DENR 2017).
Habitat destruction and unsustainable harvesting are the major global threats to orchids (Fay 2018; Gale et al. 2018). Habitat fragmentation negatively impacts species richness of orchids (Hundera et al. 2013; Parra Sánchez et al. 2016),
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and their highly specialized habit makes orchids more vulnerable to global environmental changes (Fay 2018). Orchids are also highly traded mainly for horticulture, medicine, and food (Hinsley et al. 2017). Despite being regulated under the Convention on International Trade in Endangered Species, many of the species are still being collected and traded undocumented negatively affecting wild populations around the world (Fay 2015).
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, diversity and distribution studies are still severely lacking (Buenavista 2017; Betanio and Buenavista 2018). This gap may pose conservation challenges for this highly threatened plant family, as assemblage-level studies may serve as baselines for future monitoring programs in Philippine montane ecosystems, particularly for the highly collected and traded orchids. Distribution studies also help inform species conservation assessments (e.g. IUCN Red List of Threatened Species and Philippine Red List), as these provide information on the species’ extent of occurrence and geographic range.
One of the major mountains in southern Mindanao with relatively intact lowland and montane forests is Mount Busa. It is a key biodiversity area (KBA) and one of the extremely high conservation priority sites in the Philippines (Ong et al. 2002). Portions of Mount Busa may have formed part of the older landmass of the Zamboanga Peninsula–Daguma Range block, which collided with the more recent central and eastern Mindanao blocks in the Middle Miocene, thus forming the present-day Mindanao island (Sajona et al. 1997; Hall 2002; Yumul et al. 2004). The accreted Mindanao island was intermittently connected directly to Borneo and the rest of the Sundaland through land bridges due to repeated sea-level oscillations during the Pleistocene glacial cycle (Brown et al. 2013). These events may have shaped the present-day patterns of diversity in southern Mindanao, which necessitates more field-based biodiversity studies in Mount Busa. This is relevant for orchids, as the 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 southern Mindanao remain scanty, especially for orchids in the region that do not have empirical field data yet available in published literature.
Here, we provide an inventory of orchid species found in Mount Busa with information on altitudinal and vertical distributions and their ornamental uses. Since orchid distribution is influenced by elevation and species’ traits (Jacquemyn et al. 2005; Zhang et al. 2015; Ding et al. 2016), we also examined the pattern of orchid species richness among different forest types in the area. This information helps improve our understanding of orchid diversity and
ecology and addresses the gaps in our knowledge and distribution of Philippine orchids. Our results would be helpful not only in elucidating the level of biodiversity in southern Mindanao but also in inferring patterns of plant diversity and biogeography in the Philippines.
MATERIALS AND METHODS
Study AreaWe surveyed orchid species richness along the southern slope of Mount Busa, Kiamba Municipality, Sarangani Province between July 2019 and August 2020. Mount Busa, known as “Bulul Tembob” among the local Tboli, is located at N 06°06.537’ E 124°41.026’ and reaches 2046 m in elevation, which makes it the highest point in Sarangani. It houses one of the last remaining primary forests in southern Mindanao. On 10 Mar 2020, the Provincial Government of Sarangani formally declared the southern slope of Mount Busa a local conservation area by resolution 2020-10-042.
Mount Busa was stratified into forest types based on the classification of Fernando and colleagues (2008b). We further classified the lowland evergreen forest into two: the forest ranging in elevation from 400–600 m is the MESLEF and the forest from 700–1100 m elevation is the MASLEF. The lower elevation of Mount Busa (400–1000 m) was hardly hit during the logging concession in the early 1990s, hence the dominance of secondary-growth trees at this elevation (see Brown 2015).
The forest from 1200–1600 m elevation is the LMF and from 1700–2046 m elevation is the UMF (Figure 1). Five sampling points with more than 200-m distance in between were randomly chosen in each forest type to maximize the diversity of other habitat types surveyed, although we did not limit our search to pre-defined plots. Habitats surveyed include agricultural plots of abaca, riparian areas, moist ravines, grasslands, shrublands, leaf litter, and forest trails.
Field SamplingOpportunistic sampling was done in each sampling site by four to five experienced individuals, which entailed careful and extensive examinations of understory and midstory layers of the forest for ground and epiphytic orchids. This was done with the caveat that orchid species beyond 4 m above the ground might have not been recorded due to inaccessibility or observer bias. Encountered fallen trees and branches, however, were thoroughly searched for canopy-dwelling orchids.
The altitudinal range and vertical distribution were noted for each orchid species observed in the wild. The altitude
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was recorded using a Global Positioning System (Garmin 64sc, USA), and the height at which the orchid was observed (vertical distribution) was visually estimated using the height of AJS as reference. Only flowering orchid species were included in the list. We also surveyed houses in four villages, locally called as “sitios,” around the vicinity of Mount Busa (Tulad, Datal Bong, Banate, and Green Valley) to check for orchids collected by the local people for ornamental use that we missed in the wild.
All orchid species encountered were photographed in situ whenever possible. We did not collect voucher specimens for conservation reasons. Only one or a few individuals of most species of orchids recorded were observed, and many of these species are already being collected for ornamental use. All species were identified based on photographic guides (Cootes 2001, 2011; Pelser et al. 2011 onwards), expert consultations (e.g. through the online plant identification platform of the Co’s Digital Flora of the Philippines; Barcelona et al. 2013), and taxonomic papers in orchids (Clements and Cootes 2009; Cabactulan et al. 2018).
We also checked the distribution of each identified species using the aforementioned resources. Nomenclature follows the World Checklist of Orchidaceae (Govaerts
et al. 2020), and the species’ conservation status was based on the DAO 2017-11 of the Philippine Department of Environment and Natural Resources (DENR 2017). The Philippine Department of Environment and Natural Resources (DENR) issued the fieldwork and collection permit for this study (Gratuitous Permit No. 2020-09).
Statistical AnalysisWe examined sampling adequacy using sample-size-based and coverage-based rarefaction and extrapolation (R/E) curves and a sample completeness curve for species richness (data type= incidence; Chao1). These were computed and plotted with 95% confidence intervals in the R package iNEXT (Hsieh et al. 2016). A similar analysis was used to check for orchid species richness among forest types in Mount Busa. The R/E curves allow us to evaluate sampling completeness and facilitate a conservative comparison of species richness among the forest types despite the differences in the sampling effort. Only those species observed in the wild were included in the analysis. We performed the analysis in the R statistical software Version 1.1.463 (R Core Team 2020).
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.
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Table 1. Initial list of orchid species in Mount Busa, Sarangani, Philippines.
RESULTSWe recorded 108 species of orchids from 51 genera (Table 1), at least four of which were putatively new and undescribed species – namely, Bulbophyllum sp. 3, Calanthe sp., Coelogyne sp., and Dendrochilum sp. 2. The sampling completeness curve shows that almost 50% coverage was attained for all sites (Figure 2B), suggesting that additional fieldwork would still increase the species richness of orchids, as shown in extrapolated curves (Figures 2A and 2C).
The most speciose genera were Appendicula (11.1%), Dendrobium (9.3%), and Bulbophyllum (6.5%). Fifty-three (53) species are endemic to the Philippines, of which 15 species are known only to occur in mainland Mindanao. Of the 32 orchid species that were utilized as
ornamental plants by the local people, 11 species were not observed in the wild. Only five species are threatened under the DAO 2017-11, one of which is listed as critically endangered (Grammatophyllum wallisii), three as endangered (Phalaenopsis sanderiana, Phalaenopsis reichenbachiana, Renanthera monachica), and one as vulnerable (Phalaenopsis mariae).
We report range extensions of at least nine species which are also new island records for Mindanao – namely, Thrixspermum elmeri, which was previously recorded in Negros; Cylindrolobus longissimus, Erythrodes latifolia, Rhomboda lanceolata, Blepharoglossum grossum, and Odontochilus marivelensis in Luzon; Dendrobium boosii in Luzon, Mindoro, Negros, and Leyte; Agrostophyllum loheri in Cebu, Luzon, and Samar; and Paraphaius flavus in Luzon,
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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 housebOrn. – species used as ornamental plantscWidespread – 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, which is a new locality record for the species and the first record for the Philippines (previously known to be endemic in New Guinea; confirmed by Ronny Boos and Daniel Geiger).
Most species of orchids were found in the MASLEF (700–1100 m elevation) with 39 recorded species, followed by the UMF (1700–2046 m elevation), LMF (1200–1600 m elevation), and MESLEF (400–600 m elevation) with 28, 20, and 17 recorded species, respectively (Figure 2).
Orchids showed distinct species composition among forest types, as most species were narrowly distributed. Only four species occurred in more than two forest types – namely, Dendrochilum migueldavidii, Pinalia floribunda, Spathoglottis plicata, and Thelasis carinata. The lowland evergreen forest (MESLEF and MASLEF) was mostly composed of species under the genera Appendicula, Dendrobium, and Thrixspermum (each genus had more than two species in this forest type); the LMF was dominated mainly by Bulbophyllum (four species) and Calanthe (two species but quite common along forest trails in LMF); and the UMF by the genera Dendrochilum, Phreatia, Mycaranthes, Stichorkis, and Appendicula (only A. malindangensis was found in UMF but it was the most abundant).
DISCUSSIONThe biodiversity of southern Mindanao has long been underrepresented in the scientific literature, as evinced by the lack of published studies on biodiversity in the region. Our study augments this gap and highlights the substantial level of biodiversity in southern Mindanao, particularly of the orchidaceous species which are among the most diverse yet threatened groups of plants globally and in the Philippines.
Mount Busa hosts ~ 9% of the country’s estimated number of orchid species and harbors 53+ Philippine endemic species. This estimate is higher than other surveyed montane localities in the Philippines, with twice the number of recorded species in previous studies (18–60 species; Panal et al. 2015; Buenavista 2017; Betanio and Buenavista 2018). It is even at par with the well-surveyed Samar island that has at least 90 recorded orchid species (Meneses et al. 2018). However, we acknowledge that differences in species richness estimates could be due to observer bias and differences in the sampling coverage and effort. Nevertheless, our results foreshadow the high diversity of orchids in southern Mindanao, which is worthy of conservation attention and further study.
We recorded the highest orchid species richness in the MASLEF of Mount Busa between an elevation of 700
and 1100 m, although we expect an increase in species richness in LMF and UMF (+ 1100 m elevation) with subsequent fieldwork. Several plants we observed in the montane forests did not have inflorescence or were past the flowering stage, making species identification difficult or impossible (e.g. species in the genera Ceratostylis, Crepidium, Cylindrolobus, Dendrobium, Trichoglottis, Vanda). Thus, we recommend that fieldwork should cover the flowering seasons of various genera to maximize the species inventory. On the other hand, MESLEF had the lowest number of orchid species recorded, but this estimate may increase with the addition of new sampling areas.
The larger area in MASLEF, and the associated environmental variables that are optimum for many species to survive, could explain the high species richness estimate in this forest type (species-area relationships in mountains; McCain and Grytness 2010). Our results, although inconclusive at present, suggest a mid-peak in species richness which is commonly reported in the literature (Acharya et al. 2011; Salas-Morales and Meave 2012; Zhang et al. 2015; Betanio and Buenavista 2018). However, the elevation at which the diversity peaks differs across regions. Orchid diversity in the mountains in China peak between an elevation of 1300 and 1800 m (Acharya et al. 2011; Zhang et al. 2015; Ding 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 lowland evergreen, which is the typical rainforest formation in the country (Fernando et al. 2008b).
Species composition also differed among forest types, which may be due to certain traits that allow the species to persist at certain elevations (Jacquemyn et al. 2005). This distribution pattern suggests the distinctiveness of each forest type in terms of orchid composition highlighting the importance of encompassing all forest types in management interventions, as threats differ in kind and degree across elevation. For instance, the low-elevation forests are hardly hit by habitat degradation (Soh et al. 2019) and montane organisms at all elevations are affected by climatic changes as shown in the upward migration of mountain plants, causing range contractions of narrowly distributed species (Pauli et al. 1996; Lenoir et al. 2008; Bentley et al. 2019).
Habitat degradation and climatic changes are exacerbated by the poaching and harvesting of orchid species, which remain a global threat to orchid populations (Fay 2018; Gale et al. 2018). Local collections have been observed in the villages around Mount Busa for ornamental purposes, but we found no evidence yet of trade with outside plant hobbyists and collectors. However, steps to regulate collection from the wild should be undertaken because all 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 solely observed in the villages (e.g. Phalaenopsis mariae, Phalaenopsis sanderiana, and Renanthera monachica). It is for this reason why, as a precaution, we opted not to collect species for voucher specimens since it might contribute to the reduction of orchid populations in the wild. Based on our experiences, some locals have the tendency to collect any plants that are identified as orchids, so we tried to be discreet in documenting any orchid species. If poachers can penetrate the area then this could threaten the many
diverse orchids in Mount Busa, particularly in the highly diverse lowland evergreen forest where access is easier. Species that are range-restricted, endemic, and threatened are likewise become vulnerable to poaching.
Our findings reinforce the Busa Mountain Range as a KBA and a high conservation priority site in the Philippines (Ong et al. 2002). The southern slope of the Busa Mountain Range, where our study sites are situated, has been recently 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 protection, but a designation as a protected area under the NIPAS (National Integrated Protected Areas System) may be required to instigate more conservation and scientific attention given the high level of diversity, endemism, and undescribed species in the area. Many of the KBAs in the Philippines remain unprotected (Mallari et al. 2016), which makes these areas vulnerable to illegal and unsustainable activities. Empirical field data offer strong evidence to justify protection and facilitate systematic conservation planning (Margules and Pressey 2000). Field-based biodiversity studies are particularly relevant in southern Mindanao, where threats of land conversion, mining, and illegal wildlife trade are becoming rampant.
This study provides a step towards strengthening the protection of one of the last remaining intact forests in
southern Mindanao by providing an initial list of orchids in Mount Busa, noting certain ecological traits (i.e. altitudinal and vertical distributions) that are relevant to their conservation and to future studies on orchid ecology. We recommend more distribution studies of orchids in the Philippines, particularly in montane localities, since the data are needed in many conservation interventions (e.g. monitoring, conservation planning, and species conservation assessments) and help infer phytogeographical patterns in the country. Ecological covariates that influence orchid distribution along environmental gradients should be also explored because this information remains scarce for Philippine species. The difficulty of identifying orchid species could hinder such studies, but the availability of an online platform that could connect early-career researchers (ECRs) and experts
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in the field help ameliorate this challenge (see Barcelona et al. 2013). With enough technical support to ECRs, we may be able to address many long-overdue questions in Philippine orchidology.
ACKNOWLEDGMENTSWe recorded the orchid species listed here in the course of 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 (Gratuitous Permit No. 2020-09). We are immensely grateful to Lorenzo Sinandon, tribal chieftain of the Tulad village, for sheltering us and ensuring our safety while on the field. We thank Nestor Gayan, John Timbangan,
and Dan Sulan for their significant contributions to data collection. Tristan Luap Senarillos assisted us in the literature review and John Carlo Redeña Santos created the 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) for helping us in the identification. Lastly, we thank the two anonymous reviewers who have helped in improving the early version of this manuscript.
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