Philippine Journal of Science 145 (2): 127-137, June 2016 ISSN 0031 - 7683 Date Received: ?? Feb 20??

Species Richness and Conservation Status of and Lycophytes in Mt. Hamiguitan Range Wildlife Santuary, Davao Oriental, Philippines

Victor B. Amoroso1, Fulgent P. Coritico1, and Peter W. Fritsch2

1Center for Biodiversity Research and Extension in Mindanao (CEBREM), Central Mindanao University, Musuan, Bukidnon, Philippines 2Botanical Research Institute of Texas, 1700 University Drive, Fort Worth, Texas 76107-3400, USA

An updated species list and conservation assessment of ferns and lycophytes in Mt. Hamiguitan Range Wildlife Sanctuary, Davao Oriental were provided on the basis of recent field survey and examination of herbarium specimens. One hundred and fifty-two species, belonging to 27 families and 72 genera, were recorded. The species figure is about 13% of the total number of and lycophyte species in the Philippines and nearly 20% of the total number on Mindanao Island. Twelve species are broadly distributed Philippine endemics and three more are found only on Mindanao. Nine species are new records for Mindanao. A site-endemic species, Lindsaea hamiguitanensis, was also documented. Of the 18 threatened species recorded, one is critically endangered, seven are endangered, and 10 are vulnerable.

Key words: diversity, pteridophytes, Southern Philippines, threatened species

INTRODUCTION Mt. Hamiguitan Range Wildlife Sanctuary, located in Davao Oriental Province, Mindanao, is a protected area Traditionally, pteridophytes include the so-called covering 6,834 ha between 6 °40 'N to 6 °47 'N and ferns and fern allies because of their shared life cycle 126 °09 'E to 126 °13 'E with the highest elevation of as -producing . Recently, molecular data 1,637 m a.s.l. (Karger et al. 2012). It is characterized show that pteridophytes are paraphyletic. They are by a variety of vegetation types including a unique now recognized as the lycophytes and ferns (i.e. mossy pygmy forest (Amoroso et al. 2009; Figure 1). monilophytes), the latter of which includes horsetails, It was designated as a World Heritage Site in June of whisk ferns, and all eusporangiate and leptosporangiate 2014 and is also a Mindanao Long Term Ecological ferns (Smith et al. 2006). Research Site. For the latter, extensive data collection The diversity of Philippines vascular plants includes has provided baseline information on the floral and an estimated 1,100 species of ferns and lycophytes faunal diversity in the area (Amoroso & Aspiras 2011; distributed among 154 genera and 34 families, according Amoroso et al. 2009, 2011). Nonetheless, there is no to recent classifications (e.g. Smith et al. 2006). This published checklist of ferns and lycophytes for the estimate continues to increase because of new species sanctuary. Here, such checklist is provided, along discoveries and new records in the Philippines (Amoroso with a species conservation assessment of ferns and et al. 2009; Barcelona et al. 2013). lycophytes in the sanctuary.

*Corresponding author: [email protected]

127 Philippine Journal of Science Amoroso VB et al.: Ferns and Lycophytes Vol. 145 No. 2, June 2016 of Mt. Hamiguitan

Figure 1. A. Location Map of Mt. Hamiguitan, Mindanao, Philippines; B. Transect Inventory (red line) in Mt. Hamiguitan Range Wildlife Sanctuary (Modified from DENR Region XI).

MATERIALS AND METHODS the soil, and pressing the intact. For the tree ferns, each entire frond was collected and cut into five parts: leaf apex, middle pinna, lower pinna, basal pinna, and Species Inventory stipe. All specimens were processed using the wet method An inventory of ferns and lycophytes was conducted (Hodge 1947). Herbarium specimens were deposited at through repeated transect walks from Sitio Tumalite, the Central Mindanao University Herbarium (CMUH) San Isidro, to the highest point in the sanctuary, and and, in part, at the herbarium of the California Academy down to Barangay Macambol, Mati, from 2007 to 2014. of Sciences (CAS). Another field inventory was conducted by research staff and associates at Central Mindanao University and the Species identifications are based on the specimens deposited California Academy of Sciences from 20–26 June 2015. at CMUH and were performed by consulting the following monographs, floras, and other publications: Copeland (1958- Collection, Processing, and Identification of 1961); Hovenkamp et al. (1998); Nooteboom (1998); Zhang Specimens & Nooteboom (1998); Holttum (1959a, b, c, 1978, 1981, A minimum of four fertile fronds of each species was 1991); Kramer (1971); Zamora and Co (1986) and digitized collected with a shear and trimming cutter. Small ferns plant specimens available in Global Plants on JSTOR. The were collected by uprooting the whole plant, removing classification systems used are those of Smith et al. (2006,

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2008), Rothfels et al. (2012), Labiak et al. (2014), Lehtonen Table 1. Total number of genera and species of ferns and lycophytes et al. (2010) and Hoogland & Reveal (2005). documented from Mt. Hamiguitan Range Wildlife Sanctuary. Assessments of the endangered and conservation status of the species recorded are based on the national list of threatened Number of Family Genera Number of Species Philippine plants (Fernando et al. 2008; Amoroso et al. 2015a) which follows the criteria of the International Union Aspleniaceae 1 8 for the Conservation of Nature. This information serves as a Athyriaceae 1 1 basis for governmental agencies that set environmental policy Blechnaceae 1 3 (Protected Area Management Board (PAMB), Department Cyatheaceae 2 5 of Environment and Natural Resources (DENR) and Local Davalliaceae 2 6 Government Units (LGU’s)) for monitoring and protecting threatened species, both within the sanctuary and beyond. Dennstaedtiaceae 3 3 Dicksoniaceae 1 1 Dipteridaceae 1 1 Dryopteridaceae 3 5 RESULTS AND DISCUSSION Gleicheniaceae 4 6 Hymenophylllaceae 3 11 Species Richness One hundred and fifty-two species, belonging to 27 Lindsaeaceae 3 8 families and 72 genera, were recorded. Of these, 135 Lomariopsidaceae 3 5 species are ferns and 17 are lycophytes (Tables 1 & Lycopodiaceae 2 3 2). The families with the highest number of species Lygodiaceae 1 3 are (28 species), Pteridaceae (16), Marattiaceae 2 2 Selaginellaceae (14), Hymenophyllaceae (11), and Thelypteridaceae (8). These families are also ones with Oleandraceae 1 1 the highest number of species in the entire country Ophioglossaceae 1 2 (Salgado 1990). They are also common families that are Osmundaceae 1 1 widely distributed in Mindanao (Amoroso et al. 2009, Plagiogyriaceae 1 1 2012, 2015b). Polypodiaceae 18 28 This estimate of species richness closely resembles 1 2 that of the Karst Forest in Bohol Island, Mt. Bali-it Pteridaceae 8 16 in Balbalasang-Balbalan National Park, Northern Schizaeaceae 1 3 Luzon, Mt. Marilog in the area of Davao City, and Mt. Pinamantawan in Quezon of Bukidnon Province. Selaginellaceae 1 14 It is higher than that of Mt. Iraya and its vicinity in Tectariaceae 1 5 Batan Island, Batanes Province, Mt. Pangasugan on Thelypteridaceae 5 8 Leyte Island, Pasonanca Natural Park in the region TOTAL 72 152 of Zamboanga City, and Mt. Malukot in Batangas Province, Southern Luzon. However, it is relatively lower than that of Panay Island, Mt. Burnay and its of Schizaea (commonly known as “grass fern”) in the vicinity in Northern Luzon, and two montane ecosystems Philippines (Barcelona et al. 1996) were found there: in Mindanao: Mt. Kitanglad, Bukidnon Province and viz., S. dichotoma, S. inopinata, and S. malaccana. Mt. Malindang, Misamis Occidental Province (Table The latter two species were last collected in 1923 in 3). Several factors may affect local montane species Dimyao, Bohol and in 1993 in Mt. Guiting-guiting, richness in the Philippines such as the size of the area Sibuyan Island, respectively. Other unusual species are sampled, climatic conditions, soil type, and geographic the “ant ferns” of the genus Lecanopteris. Two species location (Kessler 2010). Species richness is also affected are present, L. deparioides and L. sinuosa. The former by human activities such as the conversion of forests to was found in the pygmy forest growing epiphytically agricultural or industrial lands and pollution. on Leptospermum flavescens Sm. Two species of whisk ferns, complanatum and P. nudum, were also Noteworthy Species found, both growing on trunks of the scaly tree fern Many notable species of ferns and lycophytes were found Sphaeropteris polypoda. Nine species are new records in the sanctuary (Figure 2). Three of the four species for Mindanao: Lindsaea philippinensis (also in Luzon,

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Table 2. Checklist of ferns and lycophytes in Mt. Hamiguitan Range Wildlife Sanctuary. Aspleniaceae Asplenium affine Sw. A. nidus L. A. nigrescens Blume A. polyodon G.Forst. A. tenerum G.Forst. A. vittaeforme Cav. A. thunbergii Kunze Asplenium sp. Athyriaceae Athyrium puncticaule (Blume) T. Moore Blechnaceae Blechnum egregium Copel. B. melanocaulon (Brack.) T.C.Chambers & P.A.Farrant B. vestitum (Blume) Kuhn Cyatheaceae Alsophila fuliginosa Christ lurida (Blume) Hook. Sphaeropteris glauca (Blume) R.M.Tryon S. lepifera (J.Sm. ex Hook.) R.M.Tryon S. polypoda R.M.Tryon Davalliaceae Humata angustata (Wall. ex Hook. & Grev.) J.Sm. Humata heterophylla (Sm.) Desv. Humata repens (L.f.) Diels D. solida (G.Forst.) Sw. D. wagneriana Copel. Davallodes hirsutum (J.Sm.) Copel. Dennstaedtiaceae Histiopteris incisa (Thunb.) J.Sm. Pteridium aquilinum (L.) Kuhn Orthiopteris campylura (Kunze) Copel. var. campylura Dicksoniaceae Calochlaena javanica (Blume) Maxon Dipteridaceae Dipteris conjugata Reinw. Dryopteridaceae Bolbitis heteroclita (C.Presl) Ching Elaphoglossum callifolium (Blume) T.Moore Pleocnemia irregularis (C.Presl) Holttum P. macrodonta (Fée) Holttum P. presliana Holttum Gleicheniaceae Dicranopteris curranii Copel. D. linearis (Burm.) Underw. Diplopterygium longissimum (Blume) Nakai Gleichenia dicarpa R.Br. G. vulcanica Blume Sticherus loheri (Christ) Copel. Hymenophyllaceae Abrodictyum extravagans (Copel.) comb. ined. A. pluma (Hook.) Ebihara & K.Iwats. Cephalomanes atrovirens C.Presl Crepidomanes grande (Copel.) Ebihara & K.Iwats Crepidomanes sp.

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Table 2. continuation . . . . Hymenophyllum.acanthoides (Bosch) Rosenst. H. badium Hook. & Grev. H. denticulatum Sw. H. pallidum (Blume) Ebihara & K.Iwats H. paniculiflorum C.Presl Hymenophyllum sp. Lindsaeaceae Lindsaea apoensis Copel. L. gueriniana (Gaudich.) Desv. L. hamiguitanensis D.N.Karger & V.B.Amoroso L. obtusa J.Sm. ex Hook. L. philippinensis K.U.Kramer Odontosoria chinensis (L.) J.Sm. Odontosoria retusa (Cav.) J.Sm. Tapeinidium luzonicum (Hook.) K.U.Kramer Lomariopsidaceae Cyclopeltis crenata (Fée) C.Chr. Nephrolepis biserrata (Sw.) Schott N. cordifolia (L.) C.Presl N. hirsutula (G. Forst.) C.Presl Teratophyllum aculeatum (Blume) Mett. ex Kuhn. Lycopodiaceae Palhinhaea cernua (L.) Pic.Serm. Phlegmariurus salvinioides (Herter) Ching Phlegmariurus squarrosus (G. Forst.) A. Löve & D. Löve Lygodiaceae Lygodium flexuosum (L.) Sw. L. circinnatum (Burm.f.) Sw. L. japonicum (Thunb.) Sw. Marattiaceae Angiopteris evecta (G.Forst.) Hoffm. Ptisana sylvatica (Blume) Murdock Oleandraceae Oleandra neriiformis Cav. Ophioglossaceae Ophioderma pendula (L.) C.Presl O. reticulatum L. Osmundaceae Osmunda banksiifolia (C.Presl) Kuhn Plagiogyriaceae Plagiogyria pycnophylla (Kunze) Mett. Polypodiaceae Aglaomorpha acuminata (Willd.) Hovenkamp Ctenopterella blechnoides (Grev.) Parris Drynaria quercifolia (L.) J.Sm. D. rigidula (Sw.) Bedd. Goniophlebium mengtzeense (Christ) Rödl-Linder Lecanopteris deparioides (Ces.) Baker L. sinuosa (Wall. ex Hook.) Copel. Lemmaphyllum accedens (Blume) Donk Lepisorus longifolius (Blume) Holttum Lepisorus sp. Leptochilus decurrens Blume Loxogramme avenia (Blume) C.Presl

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Table 2. continuation . . . . Microsorum membranifolium (R.Br.) Ching M. scolopendria (Burm.f.) Copel. Oreogrammitis dolichosora (Copel.) Parris O. reinwardtii (Blume) Parris coronarium (König ex Müller) Desv. Prosaptia alata (Blume) Christ P. contigua (Forst.) C.Presl Pyrrosia lanceolata (L.) Farw. P. piloselloides (L.) M.G.Price P. samarensis (C.Presl) Ching Radiogrammitis sp. Scleroglossum pusillum (Blume) Alderw. Selliguea albidosquamata (Blume) Parris S. elmeri (Copel.) Ching S. taeniata (Sw.) Parris Themelium loherianum (Christ) Parris Psilotaceae Psilotum complanatum Sw. P. nudum (L.) Griseb. Pteridaceae Adiantum hosei Baker A. stenochlamys Baker Antrophyum immersum (Bory ex Willd.) Mett. A. latifolium Blume A. sessilifolium (Cav.) Spreng. Coniogramme macrophylla (Blume) Hieron Doryopteris concolor (Langsd. & Fisch.) Kuhn Haplopteris alternans (Copel.) Barcelona H. ensiformis (Sw.) E.H.Crane H. zosterifolia (Willd.) E.H.Crane Pteris opaca (C.Presl) J.Sm. ex Fée P. oppositipinnata Fée P. vittata L. P. whitfordii Copel. Syngramma alismifolia (C.Presl) J.Sm. Taenitis blechnoides (Willd.) Sw. Schizeaceae Schizaea dichotoma (L.) Sm. S. inopinata Selling S. malaccana Baker Selaginellaceae Selaginella agusanensis Hieron. S. alligans Hieron. S. cupressina (Willd.) Spring S. engleri Hieron. Selaginella biformis A. Braun ex Kuhn S. gastrophylla Warb.

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Table 2. continuation . . . . S. intertexta Spring S. involvens (Sw.) Spring S. jagorii Warb. S. llanosii Hieron. S. negrosensis Hieron. S. tamariscina (P.Beauv.) Spring Selaginella sp. 1 Selaginella sp. 2 Tectariaceae Tectaria crenata Cav. T. decurrens (C.Presl) Copel. T. griffithii(Baker) C.Chr. T. polymorpha (Wall. ex Hook.) Copel. T. taccifolia (Fée) M.G.Price Thelypteridaceae Christella dentata (Forssk.) Brownsey & Jermy Christella sp. Macrothelypteris polypodioides (Hook.) Holttum Nannothelypteris camarinensis Holttum Pronephrium nitidum (Holttum) Holttum P. xiphioides (Christ) Holttum Sphaerostephanos unitus (L.) Holttum Sphaerostephanos sp.

Table 3. Total number of ferns and lycophytes in different locations in the Philippines. Location Total Number of Species References Karst Forest, Bohol Island 169 Barcelona et al. 2006 Mt. Bali-it, Balbalasang- 167 Barcelona 2003a Balbalan National Park, Northern Luzon Mt. Marilog, Davao City 165 Amoroso et al. 1996 Mt. Pinamantawan, Quezon, 121 Sumagaysay 2012 Bukidnon Mt. Iraya and vicinity, Batan 89 Barcelona 2003b Island, Batanes Mt. Pangasugan, Leyte 94 Belonias and Banoc 1994 Pasonanca Natural Park, 72 Andas 2015 Zamboanga City Mt. Malukot, Batangas, 40 Catapang et al. 2012 Southern Luzon Panay Island 228 Barcelona 2004 Mt. Burnay and vicinity, 199 Iwatsuki and Price 1977 Northern Luzon Mt. Kitanglad, Bukidnon 439 Amoroso et al. 2011a Mt. Malindang, Misamis 280 Amoroso et al. 2011b Occidental

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Figure. 2. Some noteworthy species of ferns in Mt. Hamiguitan Range Wildlife Sanctuary. A. Platycerium coronarium, B. Lecanopteris deparioides, C. L. sinuosa, D. Lindsaea philippinensis, E. L. hamiguitanensis, F. Adiantum hosei, G. Schizaea dichotoma, H. S. inopinata, I. S. malaccana.

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Table 4. Conservation status of ferns and lycophytes in Mt. Hamiguitan Wildlife Sanctuary. Species Conservation Status Platycerium coronarium (König ex Müller) Desv. Critically Endangered; A1cd Alsophila fuliginosa Christ Endangered; A1cd Sphaeropteris glauca (Blume) R.M.Tryon Endangered; A1cd Lindsaea hamiguitanensis D.N.Karger & V.B.Amoroso Vulnerable, A1c Phlegmariurus salvinioides (Herter) Ching Endangered; A1c Phlegmariurus squarrosus (G. Forst.) A. Löve & D. Löve Endangered; A1c Ophioderma pendula (L.) C.Presl Endangered; A1cd Lecanopteris deparioides (Cesati) Baker Endangered; A1c, B2c Asplenium vittaeforme Cav. Vulnerable; A1cd, B2c Aglaomorpha acuminata (Willd.) Hovenkamp Vulnerable; A1c Drynaria quercifolia (L.) J.Sm. Vulnerable; A1c Microsorum scolopendria (Burm.f.) Copel. Vulnerable; A1c Psilotum complanatum Sw. Vulnerable; A1c P. nudum (L.) Griseb. Vulnerable; A1c Adiantum hosei Baker Vulnerable; A1c, B2c Doryopteris concolor (Langsd. & Fisch.) Kuhn Vulnerable; A1c, B2c Selaginella tamariscina (P.Beauv.) Spring Vulnerable; A1c Asplenium nidus L. Vulnerable; A1cd, B2c

Sibuyan, and Palawan), Pyrrosia samarensis (also in CONCLUSION Luzon and Samar), Pteris oppositipinnata (also in Abra, Neuva Ecija, Zambales, Bataan, and Rizal), Selaginella Mt. Hamiguitan Wildlife Sanctuary is home to 152 species intertexta (also in Luzon), Selaginella jagorii (also in belonging to 27 families and 72 genera. The species richness Luzon and Palawan), Tectaria taccifolia (also in Mindoro of its ferns and lycophytes flora is about 13% of the total and Palawan), Nannothelypteris camarinensis (also in number of species in the Philippines and around 20% Camarines), Schizaea inopinata (also in Bohol), and S. compared with the total number of species in Mindanao. malaccana (also in Mindoro and Sibuyan). Fifteen species are endemic to the Philippines and 9 species are new records for Mindanao Island. Eighteen threatened species are also documented. Of these, 1 species is critically Species Endemism and Conservation Assessment endangered, 7 species endangered, and 10 vulnerable. Eighteen threatened species of ferns and lycophytes were Platycerium coronarium, a critically endangered species recorded from the sanctuary. Of these, one is critically in the Philippines, is recorded in the area. endangered, seven are endangered, and 10 are vulnerable (Table 4). Fifteen Philippine endemic species of ferns and lycophytes were recorded from the sanctuary. Of these, 12 are broadly distributed Philippine endemics and ACKNOWLEDGMENTS three are restricted to Mindanao. The broadly distributed Philippine endemic species are Antrophyum sessilifolium, We thank officials of the DENR Region XI, PAMB of Lindsaea philippinensis, Nannothelypteris camarinensis, Mt. Hamiguitan Range Wildlife Sanctuary for the permit, Pleocnemia presliana, Pteris oppositipinnata, Pyrrosia Central Mindanao University (CMU), Mayor Justina Yu samarensis, Selaginella agusanensis, Selliguea elmeri, and Park Superintendent Ruel D. Colong for logistical S. intertexta, S. jagorii, S. negrosensis, and Tectaria support, and the assistance of local researchers Alfredo taccifolia. Whereas, the narrowly distributed Philippine Bolante and Leonido Clarion. This research was funded (Mindanao) endemic species are Adiantum hosei, in part by the California Academy of Sciences and the Lindsaea apoensis, and L. hamiguitanensis. The latter Commission on Higher Education of the Philippines, is also an endemic species for the sanctuary (Karger et and was conducted in partnership with U.S. National al. 2012). Science Foundation grant project DEB-1146409 (Darin S. Penneys, PI, P.W.F., co-PI).

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