Philippine Journal of Science 150 (S1): 215-221, Special Issue on Biodiversity ISSN 0031 - 7683 Date Received: 29 Sep 2020

Ophioderma subsessile (), a New Snake Tongue Species from Mindanao, Philippines

Victor B. Amoroso1,2*, Yvonne Love L. Cariño1, Joevina C. Nobleza1, and Fulgent P. Coritico1,2

1Center for Biodiversity Research and Extension in Mindanao 2Department of Biology, College of Arts and Sciences Central Mindanao University, Musuan, Bukidnon 8710 Philippines

A new species of Ophioderma, O. subsessile, is described from Mindanao, Philippines. This species is characterized by its mostly longer trophophore than sporophore, sporophore peduncle sub- sessile with a distinct sterile appendage, and strobilus longer than the peduncle. A description, illustrations, and key to the species of Philippine Ophioderma are provided.

Keywords: Mt. Pantaron Range, Ophioglossaceae, sporophore, trophophore

INTRODUCTION of Ophioderma are known from the Philippines (Holttum 1968; Copeland 1958; Barcelona 2011). The largest family of eusporangiate is the family Ophioglossaceae with 11 genera and an estimated Mt. Pantaron Range is one of the most extensive mountain 112 species (PPG I 2016; Zhang et al. 2020). Of the massifs on the Island of Mindanao and a major part of 11 genera, Ophioderma (Blume) Endl. is one of the the central Cordillera (Gronemeyer et al. 2014). This small genera consisting of four currently accepted mountain has not been fully explored botanically. In the species: Ophioderma intermedia (Hook.) Nishida, O. past years, the area revealed several species new to science simplex (Ridl. ex Brower) Nishida, O. pendula (L.) C. and a new record for the country (Gronemeyer et al. 2014; Presl, and O. redactophylla Chantanaorr. & Li Bing Coritico et al. 2017; Lagunday et al. 2017; Lagunday Zhang (Chantanaorrapint et al. 2019). Phylogenetic and Amoroso 2019). During our recent botanical survey studies have shown that Ophioderma is closely in Mt. Pantaron Range, San Fernando, Bukidnon, we related to Cheiroglossa C. Presl and distantly related encountered unusual individuals of Ophioderma growing to L. (Hauk et al. 2003; Shinohara et on a fallen decaying tree trunk. On thorough morphological al. 2013; Zhang et al. 2020). However, Cheiroglossa examination of these individuals, available type images has palmatifid or lobulated trophophore with several from JSTOR Global , the recent taxonomic key of sporophores emanating laterally on the stalk or the Chantanaorrapint et al. (2019), Barcelona et al. (2011), basal part of the trophophore while in Ophioderma, the and literature search, the characters did not match to any trophophores are simple or lobulated and the sporophores currently known described species of Ophioderma and, are single or rarely several in a serial position at the center therefore, we conclude this species is new to science. of the trophophore (Chantanaorrapint et al. 2019). The Here, we describe this new species and provide detailed highest species diversity of Ophioderma was observed in illustrations and photographs, including the key to the Southeast Asia (Wieffering 1964). Currently, two species species of Ophioderma.

*Corresponding Author: [email protected]

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MATERIALS AND METHODS Distribution and habitat: Ophioderma subsessile is known only from Mt. Pantaron at 820 m asl in lowland A botanical survey was carried out on 18–24 Aug 2020 tropical rainforest. Growing in a dense colony, this new in the lowland tropical rainforest in Mt. Pantaron, species was found thriving amongst leaf litter in fallen Bukidnon Province, Mindanao Island, Philippines. decaying tree trunk in shaded trees along with Ophioderma Voucher specimens of the new species were deposited in pendula and mat of mosses. Several individuals were the Central Mindanao University Herbarium, Philippine observed with long fleshy and soft horizontal unbranched National Herbarium, and Botanical Research Institute of roots above the decaying bark of a fallen trunk. Almost all Technology Herbarium. Freehand sections and clearing individuals were fertile during the month of August. Other techniques were done on the different parts of the plants plants around Ophioderma subsessile include Lithocarpus (including the root, trophophore, and sporophore) and spp., Shorea spp., Dillenia sp., Greeniopsis multiflora examined using stereo and compound microscopes to (Elmer) Merr., Nephrolepis cordifolia (L.) C.Presl, Scleria elucidate the morpho-anatomical features. sp., Schizaea dichotoma (L.) Sm., Selliguea taeniata (Sw.) Parris, and Piper sp. Taxonomic treatment: Ophioderma subsessile Etymology: The specific epithet “subsessile” refers to the Amoroso & Coritico, sp. nov. (Figures 1 and 2) short peduncle of the sporophore. Type: PHILIPPINES. Mindanao Island. Bukidnon: San Fernando Municipality, Mt. Pantaron Range 7°52'12.39''N 125°24'11.43'', 820 m asl (above sea level), 20 Aug 2020, Suggested common name: Pantaron Snake Tongue V.B. Amoroso & J. Nobleza 18966 (holotype: PNH! Fern. Isotypes: CMUH! BRIT!). Conservation status: Mt. Pantaron Range in Bukidnon is not yet a protected area and many threats were observed Diagnosis: This new species is similar to Ophioderma surrounding this mountain range such as illegal logging, intermedia (Hook.) Nishida but differs by its shorter small-scale mining, poaching, and over-collection of stipe and mostly longer trophophore than sporophore, biological resources. The species is found only within sub-sessile peduncle of sporophore, and strobilus longer the San Fernando part of the Pantaron Range, with an than peduncle. estimated number of 40 individuals growing on decaying Description: Plants terrestrial, 15–25 cm long, perennial logs. Thus, we recommend listing the species as critically herbs. Roots stoloniferous, horizontal, unbranched, endangered based on its very small and restricted without root hairs, brownish, soft, and fleshy, producing population with ≤ 50 mature individuals and the extent adventitious rhizome resulting in a colony with young of occurrence estimated to be < 10 km2 (IUCN Standards buds covered with sheath-like stipules. Rhizome short and Petition Committee 2019). and globose with emerging lateral white roots or aerial Taxonomic and morphological notes: The genus parts upward. Aerial parts solitary, erect, not circinate, Ophioderma was first described as a section of consisting of two parts: trophophore and sporophore; Ophioglossum L. by Blume (1828) and was subsequently sheathing stipules encircling the young bud. Trophophore raised to the generic rank by Endlicher (1936) based on erect, rarely bifurcate, narrowly attenuate, lanceolate, O. pendula (Chantanaorrapint et al. 2019). up to 25 cm long, 0.3–0.9 cm wide, pale to dark green, glabrous, undulate, margin entire, usually surpasses the We compare our new species to two other current species sporophore; stipe discernible, 3–5 cm long, gradually of Ophioderma that are most similar to its morphology merging into the lamina; basal lamina 3–4 mm wide, based on published descriptions of O. intermedia middle lamina 6–9 mm wide and upper lamina 3–6 (Wieffering 1964) and O. redactophylla (Chantanaorrapint mm wide; apex subacute to obtuse; venation reticulate et al. 2019), as well as examinations of JSTOR Type consisting of primary veins only; midrib only present in Images. Our new species is the closest morphologically to the lower part of the trophophore and continued in the O. intermedia, as shown in Table 1. The two species (O. sporophore. Sporophores 2.5–3.3 cm long, 3–4 mm wide, subsessile and O. intermedia) have similar morphological arising at the middle part of the trophophore, consisting features such as distinct stipe (hardly discernible in O. of a peduncle and a strobilus; peduncle sub-sessile, redactophylla), long trophophore up to 25 cm (up to 20 0.3–1.4 cm long; strobilus dark yellow, 1.8–2.7 cm long, cm only in O. redactophylla), and sporophore arising sterile appendage almost lacking; sporangia in two rows, about the middle of the trophophores (arising almost at 20–28 pairs, arranged alternately, opening transversely. the apex of trophophore in O. redactophylla). However, O. Spores yellowish, trilete, globose, 40–43 µm in equatorial subsessile is distinct from O. intermedia by having shorter diameter. stipe (3–5 cm long versus 4–12 cm), shorter peduncle (0.3–1.4 cm long versus 2–10 cm), trophophore longer

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Table 1. Major characteristics delineating Ophioderma subsessile from O. intermedia and O. redactophylla. O. redactophylla Chantanaorr. O. intermedia (Hook.) Nishida Characters & Li Bing Zhang O. subsessile (Wieffering 1964) (Chantanaorrapint et al. 2019) Habitat Terrestrial, growing amongst leaf Terrestrial, growing at base of Terrestrial, growing on fallen litter in lower montane forests, tree fern, dead stump of trees, decaying trunk in lowland tropical 900 m asl decaying logs rainforest, 820 m asl Root Branched, fleshy, often producing No data Unbranched, fleshy without root young buds. They referred this hairs, producing young buds one as underground parts covered with sheath-like stipules Rhizome Non-tuberous, 2 mm in diameter Subglobose, 3–4 mm Globose, 3–5 mm thick, bearing thick, bearing 1–3 fronds 1–4 fronds simultaneously Aerial part length (cm) 15–20 10–25 15–25 Stipe Hardly discernible Discernible, 4–12 cm long, Discernible, 3–5 m long, gradually merging into the lamina merging into the lamina Trophophores Lamina Flat, linear, erect Flat, lanceolate, erect, Undulate, lanceolate, erect, rarely sometimes bifurcate bifurcate Lamina length (cm) 8–15 5–15 15–25 Basal lamina width (mm) 2–2.5 2.5–3 3–4 Middle lamina width No data 5–15 6–9 (mm) Upper lamina width 3–5 5–7 3–6 (mm) Lamina base Gradually attenuate to the Attenuate Narrowly attenuate common stalk Lamina apex Acute to obtuse Acute Sub-acute to obtuse Venation Reticulate Reticulate Length of trophophore vs. Trophophore always shorter than Trophophore always shorter Trophophore mostly always longer sporophore sporophore than sporophore than sporophore Sporophores Position Arising almost at the apex of Arising at the middle part of the Arising at the middle part of trophophores trophophore trophophore Length (cm) 4.5–6.5 4.2 2.5–3.3 Peduncle length (cm) 3–4.5 2–10 0.3–1.4 Strobilus length (cm) 1.2–2 1.5–7 1.8–2.7 Strobilus width (mm) No data 2.9 3–4 Number of sporangia 15–24 pairs 36 pairs 20–28 pairs Sterile appendage Almost lacking Narrow Broad, 1–2 mm wide Spore Trilete, yellowish No data Trilete, yellowish Distribution Betong District, Yala Province Australia, New Guinea, Pantaron Range, San Fernando, Thai-Malaysia border Sumatra, Java, Borneo, Bukidnon, Philippines Philippines

(15–25 cm long versus 5–15 cm), middle trophophore With the new species, there are now a total of three narrower (6–9 mm wide versus 5–15 mm and usually species of Ophioderma known in the Philippines and trophophore surpassing the sporophore), sporophore five in Southeast Asia, viz. Ophioderma intermedia, O. shorter (2.5–3.3 cm long versus 4.2 cm), and shorter pendula, O. redactophylla, O. simplex, and O. subsessile. strobilus (up to 2.7 cm long versus up to 7 cm). The detailed morpho-anatomy of the new species shown

217 Philippine Journal of Science Amoroso et al.: Ophioderma subsessile, a New Fern Vol. 150 No. S1, Special Issue on Biodiversity Species from Mindanao, Philippines in Figures 1 and 2 revealed salient and interesting features shown in Figure 2F; 4) mesophyll region of the lamina such as: 1) the presence of arbuscular mycorrhizal is undifferentiated (Figure 2E); 5) sheath-like stipules fungi (amf) in the undulate roots and invading even the covering the bud emerging from rhizome, which has rhizome (Figures 2B and C); the amf, which are obligate been also reported in Ophioglossum by Mahabale (1962) symbionts, positively affect several aspects of plant life, and McAlpin (1971) but not reported in other species of i.e. improved nutrition, better growth, stress tolerance, Ophioderma (Figure 1E); and 6) pentacytic stomata in the and disease resistance (Chen et al. 2018); 2) protostelic lamina. Other members of the family Ophioglossaceae root and rhizome becoming dictyostelic in all parts of the exhibit a monocytic to tetracytic stomata (Mahabale frond and without sclerenchyma cells (Figures 2D-I); 3) 1962). These aforelisted features were never reported in midrib becomes distinct below the peduncle downward the literature except for the arbuscular mycorrhizal fungi (Figure 2F); it is interesting to note that the so-called in roots of Ophioglossum polyphyllum, O. nudicaule, and “midrib,” as used by Wieffering (1964), is the lower part O. gramineum, as reported by Singh et al. (2009) and in of the peduncle that is distinctly adnate to the lamina, as Ophioglossum raphaelianum (Anto et al. 2016).

Figure 1. Ophioderma subsessile: A) habit; B) globose rhizome (rh) with emerging white young root and stipe (st); C) upper surface of sporophore; D) lower surface of sporophore; E) emerging young bud (b) with visible sheath-like stipules; F) pentacytic stomata; G) proximal view of spore; H) distal view of spore.

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Figure 2. Ophioderma subsessile: A) whole plant; B–I) all cross sections except C longitudinal; B) root with arbuscular mycorrhizal fungi (amf) in middle cortex and protostelic stele; C) globose rhizome (rh) and root (r) invaded with arbuscular mycorrhizal fungi; D) stipe with dictyostele pattern of vascular bundles (vb); E) lower lamina; F. lamina (l) showing “midrib” (m); G) peduncle with five vascular bundles (vb); H) strobilus with sporangia (s); I) upper lamina with undifferentiated mesophyll (m).

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Key to species of Ophioderma (Ophioglossaceae) from the Philippines 1 Plants epiphytic with pendulous trophophores and sporophores; trophophore ribbon or strap-shaped and falcate ...... O. pendula 1 Plants always terrestrial with erect trophophore and sporophores; trophophore lanceolate and not falcate ...... 2 2 Trophophore consistently shorter than sporophore, peduncle ≥ 2 cm long; stipe long (4–12 cm long) ...... O. intermedia 2 Trophophore mostly longer than the sporophore; peduncle < 2 cm long; stipe short (3–5 cm long) ...... O. subsessile

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