New records of pteridophytes in Mount Matutum Protected Landscape, South Central Mindanao, Philippines with notes on its economic value and conservation status

: New records on distribution of pteridophytes in Mount Matutum Protected Landscape were documented. The species list was accounted with reference to specimen collections from various herbaria posted in digital databases and reliable literature on pteridophyte flora. Results further showed 105 new records for MMPL and its vicinity-South Cotabato, Sarangani province and General Santos City. From these, seven were new records for South Central Mindanao Region (Region 12). About 19 families, 56 genera were represented – 41 were epiphytes, 10 lithophytes, and 45 soil inhabitants, the rest with dual habits – two (ground and lithophytic); seven (epiphytic and lithophytic). Moreover, 11 species were found to be threatened based on national list while local conservation assessment based on relative frequency noted 91 threatened species. A conservation plan for these valuable species in the protected landscape is also proposed to ensure sound intervention and sustainable environment for this plant group.


INTRODUCTION
A significant understory flora growing in the forest reserves are the pteridophytes or the ferns and lycophytes. These plants are widely distributed both in the tropical and temperate regions especially at higher elevations, and they flourish in moist, shaded habitats (Delos Angeles & Buot 2012). They are known to have high economic value as ornaments, food, and medicine, and are noted for its high ecological importance as indicators of environmental quality (Pouteau et al. 2016;Silva et al. 2018;Khine et al. 2019). Pteridophytes are also host to diverse faunal species (Ellwood & Foster 2004;Beaulieu et al. 2010;Scheffers et al. 2014). However, its richness and diversity are continuously challenged by geogenic and anthropogenic factors that lead to fragmentation and decrease in species over the years (Rodriguez et al. 2011;Silva et al. 2018). It is then very important to know the floristics of pteridophytes in the landscape to have a better understanding on appropriate conservation interventions.
The majestic Mount Matutum Protected Landscape (MMLP) in the South Cotabato, Sarangani and General Santos (SOCSARGEN) region of southern Mindanao, is an important source of pteridophyte diversity. In fact, the entire island of Mindanao has been explored for pteridophyte diversity and about 186 species were identified (Hassler 2004(Hassler -2022. Meanwhile, 11 species were described and named bearing the epithets of mindanaoensis, mindanensis or mindanaense -Adiantum mindanaense, Alsophila mindanensis, Cyclosorus mindanaensis, Thelypteris mindanaensis, Microsorum mindanense, Polypodium mindanense, Polypodium punctatum ssp. mindanense, Polypodium punctatum var. mindanense, Selaginella mindanaoensis, Tectaria mindanaensis, and Aenigmopteris mindanaensis (Hassler 2004(Hassler -2022. Though all of these except A. mindanaense were already considered synonyms, it still highlights the significant flora in this southern part of the country. Mount Matutum was declared as protected area in 1995 through the Presidential Proclamation 552, and included in the rooster of Key Biodiversity Areas (KBAs) (Conservation International -Philippines, Haribon Foundation and the Department of Environment and Natural Resources) and Important Bird Areas (IBAs) (Birdlife International 2018) making it a priority site for conservation. It holds forest wealth of significant flora, largely unexplored that could potentially be lost together with the ecosystem services they provide, with influx of population in the surrounding communities.
Scientific studies on Mt. Matutum's biodiversity have been scarce with only a handful published accounts on trees , and bryophytes (Azuelo et al. 2016). Similarly, assessments on its faunal resource were limited to anurans (Nuñeza et al. 2017a), reptiles (Nuñeza et al. 2017b), avians (Nuñeza et al. 2019), and bats (Nuñeza et al. 2015). Until this time, these remained the only published accounts for Mt. Matutum. Interestingly, the earliest pteridophyte exploration in the protected area dates back to more than a hundred years ago (1917) by Copeland where he observed about 99 species. Among these, Gleichenia peltophora and Diplazium calliphyllum are known in the Philippines from this site only. Also, three species, though currently treated as synonyms, were named after the landscape, namely, Ctenopteris matutumensis, Dryopteris matutumensis, and Selliguea matutumensis. However, a concerted effort on documenting the Pteridophyte flora of the area remains unfinished.
The present attempt is thus the first of its kind in collating the details from various sources, including data from various herbaria and on recent field studies. It also seeks to present the economic uses associated with the pteridophytes and develop a local conservation status for each as many were not yet assessed with reference to the threatened list by the International Union for the Conservation of Nature (IUCN). As this study is the first attempt to document a more comprehensive account of the pteridophytes in the protected area, a lot of species then are new records for Mount Matutum and its vicinity -south central Mindanao region. The feature of these species is a remarkable milestone for MMPL and a significant step towards strengthening conservation interventions in the protected area. The authors seek to address the gap of an updated floristics and new records of pteridophytes in MMPL that would be crucial in their integration to conservation management as they are inevitably part of the ecosystem and function to enhance stability, resiliency, and sustainability of the landscape. This in turn cascade to the communities in form of ecosystem services, highlighting its conservation value.

Study Area
Mount Matutum Protected Landscape (MMPL) is an important landmark and ecological watershed of South Cotabato and Sarangani Provinces in Southern Mindanao. It is surrounded by four municipalities (three J TT in South Cotabato; one Sarangani Province) and 14 barangays (12 South Cotabato, two Sarangani Province). A stratovolcano, this landscape stands to about 2,286 m, covering an approximate area of 14,000 ha of forestland, with 3,000 ha of a primary forest. A community of vascular (trees, pines, ferns) and non-vascular (mosses, liverworts, hornworts) plants thrive in this this primary forest.
The climate in the northwestern and southwestern parts of this protected area is tropical with significant rainfall throughout the year even in the driest months. It is classified as Type IV with reference to Philippineclimate types and tropical wet (Af category) based on the worldwide Köppen-Geiger. Monthly temperature variations are no greater than three degrees Celsius characterized by intense surface heating and high humidity resulting to daily formation of cumulus and cumulonimbus. These conditions favor the growth of different kinds of ferns and fern allies, which greatly prefer shaded and damp habitats. Moreover, the presence of rocky environments, slopes, and host trees make this landscape a host to diverse species of pteridophytes.

Field Methods
Assessment was done following the method of Banaticla & Buot (2004) and Delos Angeles & Buot (2015). A line transect of 10─20 m, depending on the heterogeneity of pteridophyte patches, was established. At least one transect was assessed for every 100 m elevation range. All fern and lycophytes along the transect were documented including epiphytes observed below 2.5 m.
Two sites in MMPL were considered as study areas to represent its northwestern slope (Image 1). Site 1 was in the municipality of Tupi, South Cotabato, accessible through the Glandang Trail (6.3505 0 N, 125.0570 0 E) while site 2 was in the municipality of Polomolok, South Cotabato, around the Keumang-Alnamang trail (6.3300 0 N, 125.0605 0 E).
A total 92 transects were subjected for sampling, Site 1 with 52 and Site 2 with 40 transects. Composition of ferns and fern allies were listed in every transect. Voucher specimens were collected in duplicate to triplicate whenever possible. Geographic location and elevation were determined using a geographic positioning system (GPS) device.

Laboratory Methods Voucher preparation and identification
Collected specimens from MMPL were pressed and mounted in herbarium sheets.  (Copeland 1958), and others such as Ebihara et al. (2006), Lehtonen et al. (2013), Parris & Sundue (2020). Database searches were also made through Cos Digital Flora of the Philippines (Pelser et al. 2011 in www.philippineplants

Local Conservation Assessment
Local assessment of conservation was done using the relative frequency of species distribution in MMPL with reference to the work of Villanueva and Buot (2020). Relative frequency (RF) was determined by the ratio of the number of transects where the species were observed and the total number of transects. Frequency below < 0.1% was considered critically endangered (CR), > 0.1 -0.4% endangered (EN), > 0.4 -0.7 vulnerable (VU),

New Records in Mount Matutum Protected Landscape (MMPL)
Earlier studies recorded about 160 pteridophytes in Mount Matutum (Copeland 1917;Gaerlan et al. 1992;Gonzales 2001;Mindanao State University-General Santos City 2013), while this present undertaking adds another 105 taxa, totaling to 265 species in the Matutum area. Of these, 12 were lycophytes while 93 were monilophytes (ferns). As to habit, 45 were terrestrial, 41 epiphytes, 10 lithophytes and the rest showed dual habits such as terrestrial & lithophytic (two species) and epiphytic & lithophytic (seven species) ( Table 1). Copeland (1917) observed 57 ferns which were highlighted in his work on Fern Flora of the Philippines. Seventy-five years later, Gaerlan et al. (1992)  Interesting new records are the Athyrium nakanoi,   (Lehnert & Coritico 2018). Its second distribution record is in MMPL and to date, occurrence is confined to South Central Mindanao (Region 12). Abundance in MMPL of these species is marked as rare with < 5 species and frequency data of < 10%.
The species C. gracillimus, O. reinwardtii, and O. jagoriana are noteworthy records of grammitid ferns as they are not only new observations in MMPL and surrounding provinces, but also new for Region 12. They were last observed in 1904& 1909and 1904& 1924 pteridoportal.org, www.worldplants.de/worldferns). Similarly, S. ellipticus an endemic fern, is a new record for the region with type specimens found in Mindanao -Agusan & Zamboanga, from 1911─1912 collections (www.pteridoportal.org).
Also forming the new records for South Central Mindanao are Asplenium laserpitiifolium, D. geophilum, P. multicaudatum and P. celebica which were all observed in the montane forest of MMPL. There were also ferns discovered by E. Copeland in 1917 which at that time were second occurrence records in the entire Philippines -Sphaerostephanos urdanetensis, Cornopteris opaca, Cornopteris philippinensis. Meanwhile, based on worldwide database for herbarium collections, two species in Mount Matutum recorded by Copeland in 1917 remained to be the only record so far in the country namely G. peltophora and Diplazium calliphyllum.
These new records in MMPL provide significant contribution to the biodiversity heritage of Mindanao island. Prior to this study, published accounts on pteridophyte diversity has largely been from two regions -10 (Mt. Malindang & Mt. Kitanglad Range in Bukidnon) and 11 (Mt. Hamiguitan Range). The highest richness reported here was in Mt. Kitanglad Range which totalled to 439 with a total account of 632 species for the entire Mindanao island (Amoroso et al. 2011). It is expected then that the account on species richness will change with the results from this study.
Several species were also highlighted as useful either as medicine, food, or ornamental (Table 2). Tree ferns (Alsophila, Sphaeropteris) have been used as source of starch in Hawaii (Ripperton 1924;May 1978;Leach 2003) while in India it is sought from stems of giant ferns Angiopteris (Liu et al. 2012). Starch is an important product worldwide used for different purposespreservative, thickening agent, food enhancer and stabilizer and key ingredients in pastas, soups, sauces (Mason 2009;Egharevba 2019). Fern starch has been used as additive along with rice, potato and corn flour in the production of liquor and soft drinks (Liu et al. 2012). Meanwhile, fats from rhizomes have been extracted from Dryopteris which contains 90% monoethenoid (unsaturated) acids (May 1978). Medicinal ferns have been used since ancient times for common diseases -gastric, inflammatory, infections, because of the ethnobotanical knowledge on their potential as antibacterial, anti-inflammatory, diuretics and pain killers passed on to generations (Ho et al. 2010). Medicinal value was identified in Lycopodium clavatum, Selaginella involvens, Angiopteris evecta, Christella dentata, Asplenium cuneatum, and Dryopteris species while ornamental uses were featured in several Asplenium, Adiantum and, Drynaria species, and in Odontosoria chinensis and Pseudodiphasium volubile (Table 2). On the other hand, ornamental ferns have been sought to provide aesthetic value for the enjoyment of the public and potentially for environmental protection and management (Oloyede 2012) and interestingly, more money is spent for this than for all other uses (May 1978).
Notable from the list of new records is L. clavatum having been widely documented for medicinal purposes. It has been known as emetic for stomach disorders (Srivastava 2007), cure for kidney and lung diseases, analgesic, antioxidant, anti-cancer, antiinflammatory, neuroprotective, immunomodulatory, and hepatoprotective (Bhardwaj & Misra 2018). It was also explored as potent treatment for learning and memory impairment (Hanif et al. 2015). It is diuretic and anti-spasmatic and also smoked with Selaginella rupestris to cure headaches (Watt & Brandwijk 1962). In Sweden, L. clavatum is also woven into mats (May 1978).
The checklist of new records for MMPL highlights the significance of the landscape as biodiversity area in South Central Mindanao. It confirms the favorable microenvironment brought about by stable ecosystem processes in the landscape (MMPL), thereby able to house unique plants, enhancing the natural heritage. The discovery of these new records after more than 100 years, is a significant achievement, realizing that there had been few explorations in between then and now. Moreover, knowledge of species occurrence is crucial to biodiversity conservation as this provides basis for scientific-based efforts to restore diversity at its different levels (Pavlik 1995;Mehltreter 2010;Cutko 2009;Green et al. 2009;Weigelt et al. 2019). It is perceived that this study would jumpstart the continuous and regular monitoring and inventory of pteridophytes in order to aid planning, management, and policy development for the protected area. This would further lead to the inclusion of MMPL pteridophyte flora in national and worldwide botanical data and provide extensive compilation of geographic species at regional, national, and global levels.
The discovery of many economic uses of ferns and lycophytes is very instrumental to raising awareness and appreciation on the utilitarian values of this plant group. Studies to elucidate the bioactive products found in its various plant parts have led to its integration in drug discovery and potential use for various chronic and infectious diseases (Ho et al. 2010;Baskaran et al. 2018). Likewise, its ornamental values serve a pivotal role in environmental protection and management interventions and can be harnessed to improve environmental landscapes (Oloyede 2012). As the country is among the richest in pteridophyte diversity in Asia, avenues for expanding current knowledge on their utilitarian as well as ecological values are numerous, waiting to be explored.

Conservation status of the new records
With reference to IUCN Threatened List 2021, it can be grasped that all new records in MMPL belong to the Not Assessed (NA) category. The DAO-2017-11 of DENR is another reference which also integrated the national red list of threatened species (in reference to IUCN) developed in 2008 by Fernando et al. (2008). From this, a total of 11 species from new records were in the threatened category. The rest belong to other wildlife species (OWS) which refers to the native species in the landscape that were not classified to any of the threatened category. Meanwhile, seven of these new records were found to be endemic, confined only in the country.
Local assessment tool based on the relative frequency values showed a different picture as many of the OWS in DAO were placed in threatened category (Table 3). From the NA of IUCN, the OWS of DAO and native species which is roughly the least-concerned at national, and global levels, 20 were classified under CR, 44 under EN, sixVU and nine NT. Only nine species were noted to be relatively the same with least concerned status. Meanwhile, from the not threatened but endemic species (NA in IUCN, OWS in DAO and Endemic), two were found to be CR, three EN and one VU.
Under the threatened and native species category (NA in IUCN, threatened in DAO, native), one was found as CR, three were endangered, two vulnerable, one NT and four were LC. Further, the threatened and endemic category enlisted one VU and three LC species.
The local conservation status developed in this study is a simple categorical classification intended to have an immediate reference for conservation priority of pteridophyte species in MMPL. It is a vital alternative in the absence of data from IUCN which generally considers global distribution of high-valued plant species (Langenberger 2006;Villanueva & Buot 2020). As can be drawn from this study, the new records in MMPL were not yet assessed in IUCN except for one species, Sphaeropteris glauca, which was classified as least concerned. Some were also highlighted in the national list DAO 2017─11. The use of relative frequency scores could serve as reliable representation of the species' adaptation, higher RF as widely-adapted while low RF values depict restricted-range species. It is significant as in the case of MMPL which needs immediate reference as scientific information is scarce. Moreover, it can be modified in the future to include other factors that may influence their diversity and distribution such as harvest use, economic uses, threats, and other ecological factors similar to those highlighted in several works (Bacchetta et al. 2012;Rana et al. 2020;Villanueva & Buot 2020).
High priority species based on local assessment along with their endemicity and threatened status at the national level (DAO 2017─11) would serve as basis for inclusion in management plans and advocacy interventions for MMPL. Based on frequency records, these species are not widely-adapted and their elevation range is limited. Alongside that is the gradual increase of human-led activities that can potentially threaten the health of the landscape. The rise of tourist sites, plantation areas, and human settlements around MMPL, collection of wildlife species in prohibited zones, and unauthorized trekking activities in MMPL would in the long run cause degradation of the landscape. Moreover, majority of these locally threatened flora are found along montane to upper montane forest (1,600─2,000 m). As such, this study proposed for the recognition of this altitudinal range as fern biodiversity hotspot. As such, conservation programs can be focused towards the species in this zone as they could be the most sensitive to environmental changes and may in the future vanish in the landscape.

CONCLUSION
The discovery of more than one hundred new records for South Central Mindanao region and MMPL highlights its rich natural heritage and confirms its significance as key biodiversity area for pteridophytes. It is a significant addition to current botanical information as it addressed gaps in knowledge of ferns and lycophytes. The determination of conservation priority species and hotspot fern area (1,600─2,000 m) is hoped to serve as vital reference for the integration of pteridophytes in local conservation plans for MMPL.