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

Abstract

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.

Full text

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
Ophioderma subsessile (Ophioglossaceae), a New Snake
Tongue Fern Species from Mindanao, Philippines
Keywords: Mt. Pantaron Range, Ophioglossaceae, sporophore, trophophore
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.
*Corresponding Author: victorbamoroso@gmail.com
INTRODUCTION
The largest family of eusporangiate ferns is the family
Ophioglossaceae with 11 genera and an estimated
112 species (PPG I 2016; Zhang et al. 2020). Of the
11 genera, Ophioderma (Blume) Endl. is one of the
small genera consisting of four currently accepted
species: Ophioderma intermedia (Hook.) Nishida, O.
simplex (Ridl. ex Brower) Nishida, O. pendula (L.) C.
Presl, and O. redactophylla Chantanaorr. & Li Bing
Zhang (Chantanaorrapint et al. 2019). Phylogenetic
studies have shown that Ophioderma is closely
related to Cheiroglossa C. Presl and distantly related
to Ophioglossum L. (Hauk et al. 2003; Shinohara et
al. 2013; Zhang et al. 2020). However, Cheiroglossa
has palmatifid or lobulated trophophore with several
sporophores emanating laterally on the stalk or the
basal part of the trophophore while in Ophioderma, the
trophophores are simple or lobulated and the sporophores
are single or rarely several in a serial position at the center
of the trophophore (Chantanaorrapint et al. 2019). The
highest species diversity of Ophioderma was observed in
Southeast Asia (Wieffering 1964). Currently, two species
of Ophioderma are known from the Philippines (Holttum
1968; Copeland 1958; Barcelona 2011).
Mt. Pantaron Range is one of the most extensive mountain
massifs on the Island of Mindanao and a major part of
the central Cordillera (Gronemeyer et al. 2014). This
mountain has not been fully explored botanically. In the
past years, the area revealed several species new to science
and a new record for the country (Gronemeyer et al. 2014;
Coritico et al. 2017; Lagunday et al. 2017; Lagunday
and Amoroso 2019). During our recent botanical survey
in Mt. Pantaron Range, San Fernando, Bukidnon, we
encountered unusual individuals of Ophioderma growing
on a fallen decaying tree trunk. On thorough morphological
examination of these individuals, available type images
from JSTOR Global Plants, the recent taxonomic key of
Chantanaorrapint et al. (2019), Barcelona et al. (2011),
and literature search, the characters did not match to any
currently known described species of Ophioderma and,
therefore, we conclude this species is new to science.
Here, we describe this new species and provide detailed
illustrations and photographs, including the key to the
species of Ophioderma.
215
Philippine Journal of Science
150 (S1): 215-221, Special Issue on Biodiversity
ISSN 0031 - 7683
Date Received: 29 Sep 2020

MATERIALS AND METHODS
A botanical survey was carried out on 18–24 Aug 2020
in the lowland tropical rainforest in Mt. Pantaron,
Bukidnon Province, Mindanao Island, Philippines.
Voucher specimens of the new species were deposited in
the Central Mindanao University Herbarium, Philippine
National Herbarium, and Botanical Research Institute of
Technology Herbarium. Freehand sections and clearing
techniques were done on the different parts of the plants
(including the root, trophophore, and sporophore) and
examined using stereo and compound microscopes to
elucidate the morpho-anatomical features.
Taxonomic treatment: Ophioderma subsessile
Amoroso & Coritico, sp. nov. (Figures 1 and 2)
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,
V.B. Amoroso & J. Nobleza 18966 (holotype: PNH!
Isotypes: CMUH! BRIT!).
Diagnosis: This new species is similar to Ophioderma
intermedia (Hook.) Nishida but differs by its shorter
stipe and mostly longer trophophore than sporophore,
sub-sessile peduncle of sporophore, and strobilus longer
than peduncle.
Description: Plants terrestrial, 15–25 cm long, perennial
herbs. Roots stoloniferous, horizontal, unbranched,
without root hairs, brownish, soft, and fleshy, producing
adventitious rhizome resulting in a colony with young
buds covered with sheath-like stipules. Rhizome short
and globose with emerging lateral white roots or aerial
parts upward. Aerial parts solitary, erect, not circinate,
consisting of two parts: trophophore and sporophore;
sheathing stipules encircling the young bud. Trophophore
erect, rarely bifurcate, narrowly attenuate, lanceolate,
up to 25 cm long, 0.3–0.9 cm wide, pale to dark green,
glabrous, undulate, margin entire, usually surpasses the
sporophore; stipe discernible, 3–5 cm long, gradually
merging into the lamina; basal lamina 3–4 mm wide,
middle lamina 6–9 mm wide and upper lamina 3–6
mm wide; apex subacute to obtuse; venation reticulate
consisting of primary veins only; midrib only present in
the lower part of the trophophore and continued in the
sporophore. Sporophores 2.5–3.3 cm long, 3–4 mm wide,
arising at the middle part of the trophophore, consisting
of a peduncle and a strobilus; peduncle sub-sessile,
0.3–1.4 cm long; strobilus dark yellow, 1.8–2.7 cm long,
sterile appendage almost lacking; sporangia in two rows,
20–28 pairs, arranged alternately, opening transversely.
Spores yellowish, trilete, globose, 40–43 µm in equatorial
diameter.
Distribution and habitat: Ophioderma subsessile is
known only from Mt. Pantaron at 820 m asl in lowland
tropical rainforest. Growing in a dense colony, this new
species was found thriving amongst leaf litter in fallen
decaying tree trunk in shaded trees along with Ophioderma
pendula and mat of mosses. Several individuals were
observed with long fleshy and soft horizontal unbranched
roots above the decaying bark of a fallen trunk. Almost all
individuals were fertile during the month of August. Other
plants around Ophioderma subsessile include Lithocarpus
spp., Shorea spp., Dillenia sp., Greeniopsis multiflora
(Elmer) Merr., Nephrolepis cordifolia (L.) C.Presl, Scleria
sp., Schizaea dichotoma (L.) Sm., Selliguea taeniata (Sw.)
Parris, and Piper sp.
Etymology: The specific epithet “subsessile” refers to the
short peduncle of the sporophore.
Suggested common name: Pantaron Snake Tongue
Fern.
Conservation status: Mt. Pantaron Range in Bukidnon is
not yet a protected area and many threats were observed
surrounding this mountain range such as illegal logging,
small-scale mining, poaching, and over-collection of
biological resources. The species is found only within
the San Fernando part of the Pantaron Range, with an
estimated number of 40 individuals growing on decaying
logs. Thus, we recommend listing the species as critically
endangered based on its very small and restricted
population with ≤ 50 mature individuals and the extent
of occurrence estimated to be < 10 km2 (IUCN Standards
and Petition Committee 2019).
Taxonomic and morphological notes: The genus
Ophioderma was first described as a section of
Ophioglossum L. by Blume (1828) and was subsequently
raised to the generic rank by Endlicher (1936) based on
O. pendula (Chantanaorrapint et al. 2019).
We compare our new species to two other current species
of Ophioderma that are most similar to its morphology
based on published descriptions of O. intermedia
(Wieffering 1964) and O. redactophylla (Chantanaorrapint
et al. 2019), as well as examinations of Plant JSTOR Type
Images. Our new species is the closest morphologically to
O. intermedia, as shown in Table 1. The two species (O.
subsessile and O. intermedia) have similar morphological
features such as distinct stipe (hardly discernible in O.
redactophylla), long trophophore up to 25 cm (up to 20
cm only in O. redactophylla), and sporophore arising
about the middle of the trophophores (arising almost at
the apex of trophophore in O. redactophylla). However, O.
subsessile is distinct from O. intermedia by having shorter
stipe (3–5 cm long versus 4–12 cm), shorter peduncle
(0.3–1.4 cm long versus 2–10 cm), trophophore longer
Amoroso et al.: Ophioderma subsessile, a New Fern
Species from Mindanao, Philippines
Philippine Journal of Science
Vol. 150 No. S1, Special Issue on Biodiversity
216

Table 1. Major characteristics delineating Ophioderma subsessile from O. intermedia and O. redactophylla.
Characters
O. redactophylla Chantanaorr.
& Li Bing Zhang
(Chantanaorrapint et al. 2019)
O. intermedia (Hook.) Nishida
(Wieering 1964) O. subsessile
Habitat Terrestrial, growing amongst leaf
litter in lower montane forests,
900 m asl
Terrestrial, growing at base of
tree fern, dead stump of trees,
decaying logs
Terrestrial, growing on fallen
decaying trunk in lowland tropical
rainforest, 820 m asl
Root Branched, eshy, often producing
young buds. They referred this
one as underground parts
No data Unbranched, eshy without root
hairs, producing young buds
covered with sheath-like stipules
Rhizome Non-tuberous, 2 mm in diameter Subglobose, 3–4 mm
thick, bearing 1–3 fronds
simultaneously
Globose, 3–5 mm thick, bearing
1–4 fronds
Aerial part length (cm) 15–20 10–25 15–25
Stipe Hardly discernible Discernible, 4–12 cm long,
merging into the lamina
Discernible, 3–5 m long, gradually
merging into the lamina
Trophophores
Lamina Flat, linear, erect Flat, lanceolate, erect,
sometimes bifurcate
Undulate, lanceolate, erect, rarely
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
(mm)
No data 5–15 6–9
Upper lamina width
(mm)
3–5 5–7 3–6
Lamina base Gradually attenuate to the
common stalk
Attenuate Narrowly attenuate
Lamina apex Acute to obtuse Acute Sub-acute to obtuse
Venation Reticulate Reticulate
Length of trophophore vs.
sporophore
Trophophore always shorter than
sporophore
Trophophore always shorter
than sporophore
Trophophore mostly always longer
than sporophore
Sporophores
Position Arising almost at the apex of
trophophores
Arising at the middle part of the
trophophore
Arising at the middle part of
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
Thai-Malaysia border
Australia, New Guinea,
Sumatra, Java, Borneo,
Philippines
Pantaron Range, San Fernando,
Bukidnon, Philippines
(15–25 cm long versus 5–15 cm), middle trophophore
narrower (6–9 mm wide versus 5–15 mm and usually
trophophore surpassing the sporophore), sporophore
shorter (2.5–3.3 cm long versus 4.2 cm), and shorter
strobilus (up to 2.7 cm long versus up to 7 cm).
With the new species, there are now a total of three
species of Ophioderma known in the Philippines and
five in Southeast Asia, viz. Ophioderma intermedia, O.
pendula, O. redactophylla, O. simplex, and O. subsessile.
The detailed morpho-anatomy of the new species shown
Philippine Journal of Science
Vol. 150 No. S1, Special Issue on Biodiversity
Amoroso et al.: Ophioderma subsessile, a New Fern
Species from Mindanao, Philippines
217

in Figures 1 and 2 revealed salient and interesting features
such as: 1) the presence of arbuscular mycorrhizal
fungi (amf) in the undulate roots and invading even the
rhizome (Figures 2B and C); the amf, which are obligate
symbionts, positively affect several aspects of plant life,
i.e. improved nutrition, better growth, stress tolerance,
and disease resistance (Chen et al. 2018); 2) protostelic
root and rhizome becoming dictyostelic in all parts of the
frond and without sclerenchyma cells (Figures 2D-I); 3)
midrib becomes distinct below the peduncle downward
(Figure 2F); it is interesting to note that the so-called
“midrib,” as used by Wieffering (1964), is the lower part
of the peduncle that is distinctly adnate to the lamina, as
shown in Figure 2F; 4) mesophyll region of the lamina
is undifferentiated (Figure 2E); 5) sheath-like stipules
covering the bud emerging from rhizome, which has
been also reported in Ophioglossum by Mahabale (1962)
and McAlpin (1971) but not reported in other species of
Ophioderma (Figure 1E); and 6) pentacytic stomata in the
lamina. Other members of the family Ophioglossaceae
exhibit a monocytic to tetracytic stomata (Mahabale
1962). These aforelisted features were never reported in
the literature except for the arbuscular mycorrhizal fungi
in roots of Ophioglossum polyphyllum, O. nudicaule, and
O. gramineum, as reported by Singh et al. (2009) and in
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.
Amoroso et al.: Ophioderma subsessile, a New Fern
Species from Mindanao, Philippines
Philippine Journal of Science
Vol. 150 No. S1, Special Issue on Biodiversity
218

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).
Philippine Journal of Science
Vol. 150 No. S1, Special Issue on Biodiversity
Amoroso et al.: Ophioderma subsessile, a New Fern
Species from Mindanao, Philippines
219

ACKNOWLEDGMENTS
The authors are grateful to the Department of Science
and Technology –Grants-In-Aid for funding this research.
We thank the Department of Environment and Natural
Resources – Region X Office for the issuance of the
Gratuitous Permit No. 2020-06; the Philippine Council
for Agriculture, Aquatic, and Natural Resources Research
and Development for monitoring the research; the local
government officials and indigenous peoples (Manobo
Matig-langilan and Manobo Matig-salog) of San Fernando,
Bukidnon; and the administration of Central Mindanao
University led by Dr. Jesus Antonio G. Derije for logistical
support during the conduct of this botanical survey.
REFERENCES
ANTO PB, KHAN A, FRANCIS F, ANTONY I. 2016.
Opohioglossum raphaelianum (Ophioglossaceae) – A
New Species from South India. International Journal
of Advanced Research 4(5): 1268–1273.
BARCELONA JF. 2011 onwards. Pteridophytes (Lyco-
phytes and Monilophytes). In: Co's Digital Flora of the
Philippines. Pelser PB, Barcelona JF, Nickrent DL eds.
BLUME CL. 1828. Enumeratio plantarum Javae et insu-
larum adjacentium: minus cognitarum vel novarum ex
herbariis Reinwardtii, Kuhlii, Hasseltii et Blumii. J.W.
van Leeuwen, Leiden [Lugduni Batavorum]. 276p.
CHANTANAORRAPINT S, PETCHSRI S, ZHANG L,
ZHANG L. 2019. Ophioderma redactophylla (Ophio-
glossaceae), a new fern from the Malay Peninsula.
Phytotaxa 422: 101–105.
CHEN M, ARATO M, BORGHI L, NOURI E, REIN-
HARDT D. 2018. Beneficial Services of Arbuscular
Mycorrhizal Fungi – From Ecology to Application.
Frontiers in Plant Science 9: 1–14.
Key to species of Ophioderma (Ophioglossaceae) from the Philippines
1Plants epiphytic with pendulous trophophores and sporophores; trophophore ribbon
or strap-shaped and falcate .......................................................................................... O. pendula
1Plants always terrestrial with erect trophophore and sporophores; trophophore
lanceolate and not falcate ............................................................................................ 2
2Trophophore consistently shorter than sporophore, peduncle ≥ 2 cm long; stipe long
(4–12 cm long) ............................................................................................................. O. intermedia
2Trophophore mostly longer than the sporophore; peduncle < 2 cm long; stipe short
(3–5 cm long) ............................................................................................................... O. subsessile
COPELAND E. 1958. Fern flora of the Philippines. Vol.
1–3. Manila Bureau of Printing. p. 1–555.
CORITICO FP, AMOROSO VB, LEHNERT M. 2017.
New records, names and combinations of scaly tree
ferns (Cyatheaceae) in eastern Malesia. Blumea 62:
92–96.
ENDLICHER SL. 1936. Genera plantarum secundum or-
dines naturales disposita. F. Beck, Vindobonae. 1484p.
GRONEMEYER T, CORITICO FP, WISTUBA A, MAR-
WINSKI D, GIERAY T, MICHELER M, MEY FS,
AMOROSO VB. 2014. Four new species of Nepenthes
L. (Nepenthaceae) from the central mountains of Min-
danao, Philippines. Plants 3(2): 284–303.
HAUK WD, PARKS CR, CHASE MW. 2003. Phyloge-
netic studies of Ophioglossaceae: Evidence from rbcL
and trnL-F plastid DNA sequences and morphology.
Molecular Phylogenetics and Evolution 28: 131–151.
HOLTTUM RE. 1968. A Revised Flora of Malaya, Vol.
2, Ferns of Malaya. U.S. Government Printing Office,
Singapore. 653p.
IUCN STANDARDS AND PETITIONS COMMITTEE.
2019. Guidelines for Using the IUCN Red List Cat-
egories and Criteria, Version 14. Retrieved from http://
www.iucnredlist.org/documents/RedListGuidelines.
pdf
LAGUNDAY NE, ACMA FM, CABANA VG, SABAS
NM, AMOROSO VB. 2017. Two new Nepenthes
species from the unexplored mountains of central
Mindanao, Philippines. Philippine Journal of Science
146: 159–165.
LAGUNDAY NE, AMOROSO VB. 2019. Nepenthes ca-
banae (Caryophyllales, Nepenthaceae), a new species
of pitcher plant from Central Mindanao, Philippines.
Philippine Journal of Systematic Biology 13: 39–45.
Amoroso et al.: Ophioderma subsessile, a New Fern
Species from Mindanao, Philippines
Philippine Journal of Science
Vol. 150 No. S1, Special Issue on Biodiversity
220

MAHABALE TS. 1962. Species of Ophioglossum in
India: Their Taxonomy and Phylogeny. Bulletin of the
Botanical Survey of India 4(1–4): 71–84.
MCALPIN BW. 1971. Ophioglossum Leaf Sheaths: De-
velopment and Morphological Nature. Bulletin of the
Torrey Botanical Club 98(4): 194–199.
PPG I. 2016. A community‐derived classification for
extant lycophytes and ferns. Journal of Systematics
and Evolution 54: 563–603.
SHINOHARA W, NAKATO N, YATABE-KAKUGAWA
Y, OKA T, KIM JK, MURAKAMI N, NODA H, SA-
HASI N. 2013. The use of matK in Ophioglossaceae
phylogeny and the determination of Mankyua chro-
mosome number shed light on chromosome number
evolution in Ophioglossaceae. Systematic Botany 38:
564–570.
SINGH A, MISHRA S, GUPTA S, BEHERA S, PREM
K. 2009. Studies on the Genus Ophioglossum L. in
Pachmarhi Biosphere Reserve, Madhya Pradesh-India.
Taiwania 54: 353–364.
WIEFFERING JH. 1964. A preliminary revision of the
Indo-Pacific species of Ophioglossum (Ophioglos-
saceae). Blumea 12: 321–337.
ZHANG L, FAN X-P, PETCHSRI S, ZHOU L, POLLA-
WATN R, ZHANG X, ZHOU X-M, LU NT, KNAPP
R, CHANTANAORRAPINT S, LIMPANASIT-
TICHAI P, SUN H, GAO X-F, ZHANG L-B. 2020.
Evolutionary relationships of the ancient fern lineage
the adder’s tongues (Ophioglossaceae) with description
of Sahashia gen. nov. Cladistics 36: 380–393.
Philippine Journal of Science
Vol. 150 No. S1, Special Issue on Biodiversity
Amoroso et al.: Ophioderma subsessile, a New Fern
Species from Mindanao, Philippines
221