THREATENED LYCOPHYTES AND FERNS IN FOUR PROTECTED AREAS OF MINDANAO, PHILIPPINES

There are nearly a thousand threatened species of vascular plants in the Philippines and of which about 12% are lycophytes and ferns. However, there are not enough data on the distribution of the species. Thus, the threatened lycophytes and ferns were determined based on field surveys in four protected areas in Mindanao, namely Mt. Apo Natural Park, Mt. Kitanglad Range Natural Park, Mt. Malindang Range Natural Park, and Mt. Hamiguitan Range Wildlife Sanctuary. The conservation status assessment was based on the Department of Environment and Natural Resources DAO 2017-11 updated list of threatened plants of the Philippines. A total of 45 species of threatened lycophytes and ferns was documented belonging to 16 families and 25 genera. Of these, three species are Critically Endangered, 23 Endangered, 15 Vulnerable, and three are other threatened species. Families with the highest number of threatened species are Cyatheaceae, Polypodiaceae, Lycopodiaceae, Ophioglossaceae, and Psilotaceae. The Critically Endangered species are Platycerium coronarium, Phlegmariurus magnusianus, and Helminthostachys zeylanica. The threatened species endemic to the Philippines are Phlegmariurus magnusianus, Alsophila apoensis, A. atropurpurea, A. hermannii, A. fuliginosa, A. heterochlamydea, A. negrosiana, A. rufopannosa, Lindsaea hamiguitanensis, Tmesipteris zamorarum, Aglaomorpha cornucopia, and A. sagitta. The highest number of threatened taxa was observed in the Mt. Apo Natural Park (29 species), followed by the Mt. Kitanglad Range Natural Park (28 species), Mt. Malindang Range Natural Park (27 species), with the lowest number in the Mt. Hamiguitan Range Wildlife Sanctuary (19 species). Most of the species were recorded in the lower and upper montane forests. The occurrence of threatened and endemic lycophytes and ferns in the four protected areas calls for a strict implementation of the ordinances necessary for a long term conservation and protection of the species.


Introduction
Pteridophytes include the so-called ferns and fern allies, the latter so-called because of their shared life cycle as spore-dispersing vascular plants (Amoroso et al., 2016a,b). However, recent analyses of morphological and molecular data revealed that pteridophytes are paraphyletic, and the boundary within them has been withdrawn to distinguish lycophytes and ferns (monilophytes) (Smith et al., 2006;PPG I, 2016). There are 11 916 estimated species of ferns and lycophytes throughout the world (PPG I, 2016). About 4500 species occur in Southeast Asia, which is more than one third of the world diversity (Moran, 2008;Ebihara et al., 2012). In the Philippines, there are 1100 species of lycophytes and ferns distributed among 154 genera and 34 families (Barcelona, 2011(Barcelona, -2020Amoroso et al., 2016b) and ca. 632 species (57%) are found on Mindanao Island (Amoroso et al., 2009).
Mindanao Island is the second largest island in the Philippine archipelago and has an enormous numbers of endangered, endemic and economically important species of flora and fauna. This island has a total of 41 Protected Areas (PAs) classified as national parks, natural parks, natural monuments, protected landscapes and seascapes, resource reserves, wildlife sanctuaries, marine reserves, watershed forest reserves, natural biotic areas, and wilderness areas based on the National Integrated Protected Areas System (NIPAS) Act of 1992.
Mt. Apo Natural Park (MANP), Mt. Kitanglad Range Natural Park (MKRNP), Mt. Malindang Range Natural Park (MMRNP) and Mt. Hamiguitan Range Wildlife Sanctuary (MHRWS) are some of the Protected Areas in Mindanao Island. These mountain ecosystems are also considered as ASEAN Heritage Parks. Moreover, MHRWS was listed as a UNESCO World Heritage site in 2014. All of these four Protected Areas are also Philippine Long-Term Ecological Research (LTER) sites (Kim et al., 2017) and home to different endemic species of plants and animals (Amoroso et al., 2009;Mohagan et al., 2015Mohagan et al., , 2018Amoroso et al., 2015Amoroso et al., , 2018. Initial listing of the plants in the area was provided by Amoroso et al. (2006) in Mt. Malindang, Amoroso et al. (2009) in Mt. Hamiguitan, and Amoroso et al. (2011) in Mt. Kitanglad. A list of the threatened plant species on Mindanao Island was provided by Lumista et al. (2016) and Aribal & Buot (2009). Also, Fernando et al. (2008) listed 202 species of ferns and lycophytes as nationally threatened in the Philippines. However, their list did not provide complete information about the distributions of the species on Mindanao and they followed the old assessment of the Department of Environment and Natural Resources (DENR).
Thus, this paper provides a comprehensive and updated list of threatened lycophytes and ferns, species conservation assessment, their distribution through field validation in the four selected Protected Areas on Mindanao, Philippines. This paper serves as basis for strict protection and conservation of the remaining threatened endemic species of lycophytes and ferns in the four Protected Areas on Mindanao Island.

Species inventory
Prior to the conduct of the field work, a gratuitous permit from the four Protected Areas on Mindanao was obtained from the DENR regional offices. An inventory of lycophytes and ferns was then conducted by the authors from January 2014 to December 2015 through repeated transect walks from the foot of the mountain to the highest point in Mt. Apo Natural Park, North Cotabato (125.275000° N, 7.260833° E), Mt. Kitanglad Range Natural Park, Bukidnon (124.916700° N, 5.083333° E), Mt. Malindang Range Natural Park, Misamis Occidental (123.600000° N, 8.283333° E), and Mt. Hamiguitan Range Wildlife Sanctuary, Davao Oriental (126.166700° N, 6.716666° E) (Fig. 1). Another field inventory was conducted by researchers from Central Mindanao University and the Botanical Research Institute of Texas from 2016 to 2019. These sites were selected because they are considered as Long Term Ecological Research (LTER) sites on Mindanao and also designated as ASEAN Heritage Parks.

Collection, processing, and identification of specimens
A minimum of two fertile fronds of each species was collected and processed using the wet method (Hodge, 1947). All herbarium specimens were deposited at the Central Mindanao University Herbarium (CMUH) and the California Academy of Sciences (CAS). All the specimens were identified by the authors using monographs, e-floras and other publications like Copeland (1958), the Flora Malesiana Series and digitised plant specimens available in Global Plants on JSTOR (https://plants.jstor.org/). The classifications were based on PPG I (2016).

Assessment of the conservation status and distribution
The assessment of the conservation status of the species was based on the updated national list of threatened plants in the Philippines, following the criteria for determination of threatened plant species and their categories of the Department of Environment and Natural Resources (DENR-DAO, 2017). The categories are as follows: Critically Endangered (CR), Endangered (EN), Vulnerable (VU) and Other Threatened Species (OTS), which is equivalent to Near Threatened of the International Union for Conservation of Nature (IUCN). This is the latest assessment on the national list of threatened plants in the Philippines made by the Philippine Plant Conservation Committee (PPCC) organised by DENR. The assessments of the conservation status of the species in the country are updated every five years. Information from this list serves as the basis for national environmental policy for the Protected Area Management Board (PAMB) of the Protected Areas and Local Government Units (LGUs) for strictly monitoring and protecting the endangered plant species. The general data on the distribution of species outside the four Protected Areas was based on Barcelona (2011Barcelona ( -2020 and Lindsay & Middleton (2012, with data for some species complemented by field observations of the authors.

Species richness
A total of 45 species, six species of lycophytes and 39 of ferns, in the four Protected Areas are threatened, comprising 16 families and 25 genera. The families with the highest number of threatened taxa are Cyatheaceae (ten species), Polypodiaceae (nine species), Lycopodiaceae (five species), and Ophioglossaceae and Psilotaceae with three species each. In these families, some species have high economic importance as ornamental and medicinal plants (Amoroso, 2013;Magtoto & Austria, 2017). Of the 45 species recorded in the four Protected Areas on Mindanao, three species are considered as Critically Endangered taxa, 23 Endangered, 15 Vulnerable and three Other Threatened Species (Table).

Critically Endangered species
Platycerium coronarium (König ex Müller) Desv. Platycerium coronarium is a common, ornamental plant characterised by strongly dimorphic fronds with dichotomous nest leaves and pendulous dichotomously branched fertile fronds ( Fig.  2A). It is commonly sold in flower gardens in big cities like Cagayan de Oro City and Davao City on Mindanao and Manila City on Luzon for a very expensive price. This species is considered as Critically Endangered because of its limited distribution in the wild and over-collection as an ornamental plant. In this study, it was observed only within the Mt. Hamiguitan Range Wildlife Sanctuary, Davao Oriental as an epiphyte on Shorea polysperma Merr. and Tristaniopsis de- However, a new population of P. coronarium has recently been discovered by the authors in the Mt. Pantaron Range, Bukidnon in Central Mindanao, which is not a Protected Area.

Phlegmariurus magnusianus (Herter) A.R.Field & Testo
Phlegmariurus magnusianus (Lycopodiaceae) is an epiphytic fern with pendulous stems, which are twice to three times isodichotomously branched, and with narrow-lanceolate, acuminate crowded leaves arranged in close spirally whorled (Fig. 2B). Species in this family are locally known as «salindugok or ikog sa iring», and commonly harvested by the local people in different parts of the country and sold very cheaply. This species was found in Mt. Apo Natural Park and Mt. Malindang Range Natural Park where it grows epiphytically on trees at about 3-10 m high. Only a few individuals of this species were observed.
Distribution. This species is endemic to the Philippines, known from Luzon and Mindanao (Mt. Apo Natural Park and Mt. Malindang Range Natural Park). Helminthostachys zeylanica (L.) Hook.
Helminthostachys zeylanica (Ophioglossaceae) is a herbaceous fern usually with a solitary frond and a fertile spike that arises from the base of its frond (Fig. 2C). This species is locally known as «tungkod-langit» and generally found at lower altitudes on wet and muddy places. It was recorded only in Mt. Malindang Range Natural Park for this study.
In some countries like Brunei, it is commonly sold at the market as vegetables and medicine (de Winter & Amoroso, 2003). However, there are no reports from the Philippines that this species is edible.
Distribution. This species is widely distributed in the Palaeotropics, from Sri Lanka and India (Assam) to New Caledonia and Australia. Philippines: Palawan and Mindanao (Mt. Malindang Range Natural Park).

Threatened and endemic species of Mindanao
Alsophila hermannii R.M.Tryon Alsophila hermannii is a medium-size scaly tree fern of the family Cyatheaceae. Trunks are erect to 4(-6) m height, to 24-27 cm diameter with old petiole bases and with marginate light to dark brown scales (Fig. 2D). The species was known only from its type locality on Mt. Apo. However, our study recorded this species in the Mt. Kitanglad Range Natural Park growing in the upper montane to the mossy forests (2000-2300 m a.s.l.).

Alsophila rufopannosa (Christ) R.M.Tryon
Alsophila rufopannosa (Cyatheaceae) is a fern endemic to Mindanao Island. It is also a medium size tree fern with trunks erect to 4(-6) m height, and to 15-18 cm diameter, without old petiole bases and with numerous marginate reddish brown scales on petioles and rachises (Fig. 2E)

Lindsaea hamiguitanensis D.N.Karger & V.B.Amoroso
Lindsaea hamiguitanensis is a small herbaceous fern with triangular, bipinnate to tripinnatepinnatifid fronds that are light green when dry, with reddish brown and quadrangular rachises (Fig. 2F) In total there are 291 endemic species of ferns and lycophytes in the Philippines (Barcelona, 2011(Barcelona, -2020, with about 94 of them considered also by DAO 2017-11 as threatened. In this study, the threat- The family Cyatheaceae has the most threatened endemic species, with 70% of the total number of the scally tree ferns recorded. All species in this tree fern family are listed in the Convention on Interna-tional Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix II in which the species are not necessarily threatened with extinction, but their trade must be controlled in order to avoid utilisation incompatible with their survival.
Other threatened ferns found on the study sites are species of Psilotaceae, Schizaeaceae, Lecanopteris, Selaginella tamariscina (P.Beauv.) Spring and Ophioderma pendula C.Presl. Members of the family Psilotaceae are unusual looking ferns that are rootless and sometimes leafless as in Psilotum. In the Philippines, all of the Psilotaceae species are considered as threatened, namely Psilotum nudum (L.) P.Beauv. (VU) (Fig. 3A), Psilotum complanatum Sw. (EN) and Tmesipteris zamorarum (EN) (Fig. 3B). Psilotum nudum and P. complanatum were observed growing on tree fern trunks of Sphaeropteris polypoda (Baker) R.M.Tryon in Mt. Hamiguitan Range Wildlife Sanctuary. Tmesipteris zamorarum also grows only on tree fern species trunks of Cyatheaceae and Dicksoniaceae. This species was recorded only in high mountain ecosystems above 2000 m a.s.l., such as Mt. Apo Natural Park, Mt. Kitanglad Range Natural Park and Mt. Malindang Range Natural Park. There are five Schizaeaceae species reported in the Philippines. All of these are found in Mt. Hamiguitan Range Wildlife Sanctuary (Amoroso et al., 2020). Two species are considered as Endangered, namely Actinostachys inopinata (Selling) C.F.Reed (Fig. 3C) and Schizaea malaccana Baker. These species are found in forests on ultramafic soil in Mt. Hamiguitan Range Wildlife Sanctuary, growing together with Schizaea dichotoma (L.) Sm. Two species of «ant ferns» of the genus Lecanopteris are present, namely L. deparioides (Ces.) Baker and L. sinuosa (Hook.) Copel. (Fig.  3D). These species are epiphytes on trees, like Leptospermum polygalifolium Salisb. subsp. polygalifolium, Sphaeropteris spp. Lecanopteris deparioides was recorded in Mt. Hamiguitan Range Wildlife Sacntuary and Mt. Malindang Range Natural Park while L. sinuosa was found only in Mt. Hamiguitan Range Wildlife Sanctuary.
Selaginella tamariscina (Fig. 3E) is the only threatened species in the family Selaginellaceae recorded in the four Protected Areas. It is known for its antibacterial, anticancer, antifungal, and antiviral activities (Gechev et al., 2014). It is widely used by the local people in the Philippines to cure diseases (Setyawan, 2009;Amoroso, 2013). Thus, there is over-exploitation of this species in the wild. This species was recorded only in the eastern side of Mt. Hamiguitan Range Wildlife Sanctuary near the river banks growing on rocks and boulders. Ophioderma pendula or «ribbon» fern (Fig. 3F) was recorded in all four Protected Areas on Mindanao. The species is also commonly harvested by the local people in the Philippines and sold cheaply. Most of the species were included in the threatened list of plants for the Philippines because they are widely collected in the wild for their ornamental and medical uses, thus, depleting the population of the species.

Discussion
There are many reasons why species become threatened or endangered. Habitat destruction through logging, shifting cultivation, land use/ land cover change, environmental pollution, invasive species, grazing, urbanisation, hydrological disturbance, and over-exploitation of forest resources are considered as the major threats to biodiversity worldwide (Catibog-Sinha & Heaney, 2006;Amoroso et al., 2011;Monastersky, 2014;Khapugin et al., 2020). Climate change is also one of the primary causes of species endangerment (Ibrahim et al., 2013). Moreover, plants are also becoming extinct because of distinctive sequential patterns, with agriculture, invasions, and urbanisation as significant drivers in hotspots, whereas hydrological disturbance is an important driver in coldspots (Le Roux et al., 2019).
The recent assessment of DENR was primarily based on the IUCN criteria applied to infor-applied to information from scientific literature (e.g. geographic distribution of the species, extent of area of occupancy, actual threats of habitat, and over exploitation of high economic or commercial value species), available herbarium specimens, biodiversity survey data and Filipino botanists' field experience and knowledge of the flora.
Most of the threatened lycophytes and ferns (71%) are found in mountain ecosystems in different parts of the country. Mt. Apo Natural Park had the highest number of taxa with 29 species, followed by Mt. Kitanglad Range Natural Park (28 species), Mt. Malindang Range Natural Park (27 species), and Mt. Hamiguitan Range Wildlife Sanctuary (19 species). The high number of threatened species in Mt. Apo and Mt. Kitanglad is caused by the diversity of vegetation types in the area like the upper and lower montane forests (Amoroso et al., 2011(Amoroso et al., , 2016b. Most of the threatened tree ferns and lycopods are found in this vegetation type. Most of the threatened lycophytes and ferns (53%) inhabited the lower and upper montane forests with an altitude range of 1000-1500 m a.s.l. and 1500-2300 m a.s.l., respectively, followed by the lowland forests (< 1000 m a.s.l.), and the mossy forests (above 2300 m a.s.l.) (Table, Fig. 4). Species richness of ferns and lycophytes increased with altitude (Acebey et al., 2017). The highest species richness of ferns in the montane forests supports the findings of Bhattarai et al. (2004), Kluge et al. (2006), Kessler et al. (2011), Salazar et al. (2015 that fern richness was the highest in mid-altitudes, usually in montane forests. This has often been linked to an optimal combination of high humidity, rainfall, and moderate temperatures at mid-altitudes (Lauer et al., 1996).  (Barcelona et al., 2006), Aglaomorpha splendens, Platycerium coronarium, Phlegmariurus squarrosus (G.Forst.) Á.Löve & D.Löve, Sphaeropteris glauca in Mindoro Island (Villanueva & Buot, 2015).

Conclusions
The presence of threatened lycophytes and ferns on the study sites should be given high priority for conservation and action by the government to prevent their extinction. Communication, education and public awareness about fern diversity and its importance should be done to enhance the awareness of the local communities and of the public in general. Propagation protocols should also be developed to mass propagate these threatened and endemic species of lycophytes and ferns. A complete database about the distribution of threatened lycophytes and ferns in the Philippines should be prepared for easy monitoring of the species. Finally, effective forest management and strict implementation of the ordinances are necessary for the long term conservation and protection not only to lycophytes and ferns but the whole flora and fauna within these Protected Areas.