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Explorations on the knowledge and biodiversity of Philippine lichen fungi have progressed recently. However, comparatively little attention has been given to the species composition along a lowland secondary forest ecosystem. Thus, the study aimed to provide information on the occurrence of lichen species in relation to various land use types of Mt. Musuan of Mindanao Island, surrounded by forest fragments and cultivated agricultural areas. A series of transect walks and opportunistic sampling revealed a total of 38 lichen species distributed in 26 genera and 14 families. Among the land use types, the mixed species forest harbors the highest recorded species with 22, followed by teak forest and built-up (peak/summit) with 15 and 14 species, respectively. Lichens with the most represented families were revealed to be Graphidaceae with 10 species; Caliciaceae with six species; Physciaceae, Parmeliaceae, and Arthoniaceae with three species each; and Pyrenulaceae, Collemataceae, Letrouitiaceae, and Trypetheliaceae with two species each. Out of these collections, two species-viz. Letrouitia subvulpina (Nyl.) Hafellner and Pyrenula globifera (Eschw.) Aptroot-were new records in the Philippines. The results of this study will provide information to encourage effective management and biodiversity conservation efforts of various land use types, as lichens are sensitive to anthropogenic threats and pressures from environmental conditions.
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2077
Lichens across Land Use Types of Mt. Musuan,
Bukidnon, Southern Philippines
Ermalene C. Taer1*, Manuela Dal Forno2,3, Bibiana Moncada4,5,6,
Victor B. Amoroso1,7, and Fulgent P. Coritico1,7
1Plant Biology Division, Institute of Biological Sciences, College of Arts and Sciences,
Central Mindanao University, University Town, Musuan, Bukidnon 8710 Philippines
2Botanical Research Institute of Texas, Fort Worth Botanic Garden,
Fort Worth, Texas 76107 United States
3Department of Botany, Smithsonian Institution, National Museum of Natural History,
10th St. & Constitution Ave. NW, Washington, District of Columbia 20560 United States
4Botanischer Garten, Freie Universität Berlin, Königin-Luise-Straße 6-8, 14195 Berlin, Germany
5Negaunee Integrative Research Center, The Field Museum,
1400 South Lake Shore, Chicago, Illinois 60605 United States
6Biología y Licenciatura en Biología, Universidad Distrital Francisco José de Caldas,
Cra. 4 No. 26D-54, Torre de Laboratorios, Herbario, Bogotá, Colombia
7Center for Biodiversity Research and Extension in Mindanao,
Central Mindanao University, University Town, Musuan, Bukidnon 8710 Philippines
Explorations on the knowledge and biodiversity of Philippine lichen fungi have progressed
recently. However, comparatively little attention has been given to the species composition along
a lowland secondary forest ecosystem. Thus, the study aimed to provide information on the
occurrence of lichen species in relation to various land use types of Mt. Musuan of Mindanao
Island, surrounded by forest fragments and cultivated agricultural areas. A series of transect
walks and opportunistic sampling revealed a total of 38 lichen species distributed in 26 genera
and 14 families. Among the land use types, the mixed species forest harbors the highest recorded
species with 22, followed by teak forest and built-up (peak/summit) with 15 and 14 species,
respectively. Lichens with the most represented families were revealed to be Graphidaceae with
10 species; Caliciaceae with six species; Physciaceae, Parmeliaceae, and Arthoniaceae with three
species each; and Pyrenulaceae, Collemataceae, Letrouitiaceae, and Trypetheliaceae with two
species each. Out of these collections, two species – viz. Letrouitia subvulpina (Nyl.) Hafellner
and Pyrenula globifera (Eschw.) Aptroot – were new records in the Philippines. The results
of this study will provide information to encourage effective management and biodiversity
conservation efforts of various land use types, as lichens are sensitive to anthropogenic threats
and pressures from environmental conditions.
Keywords: Mindanao, new record, non-vascular, secondary forest, species richness
*Corresponding author: s.taer.ermalene@cmu.edu.ph
Philippine Journal of Science
152 (6A): 2077-2086, December 2023
ISSN 0031 - 7683
Date Received: 15 Jun 2023
2078
INTRODUCTION
The Philippines is a biodiversity hotspot home to 1262
lichen species (Paguirigan et al. 2020) and a repository
of diversely unique natural biota with a high level of
endemism and many threatened and endangered species
(Amoroso et al. 2012). Explorations on the knowledge and
biodiversity of Philippine lichen fungi have progressed
recently [e.g. Fajardo and Bawingan (2019); Lucban and
Paguirigan (2019); Paguirigan et al. (2019); Bawingan et
al. (2019, 2022)]. However, critical threats due to habitat
loss are faster than ever, pushing poorly understood
species to the brink of extinction before they are even
discovered.
Within greater Mindanao, for instance, explorations
have been conducted – highlighting the descriptions and
biodiversity patterns of lichens in a mountain ecosystem
with multiple vegetation types and elevational gradients
(Azuelo and Puno 2018; Cababan et al. 2020; Magday et
al. 2020). Nonetheless, the aforementioned observations
may not be readily applicable to a secondary forest
ecosystem situated in lowland areas, where abiotic factors
such as limited humidity and light gradient may not result
in significant stratification of species distribution (Benzing
1990; Graham and Andrade 2004) and reduced forest
cover attributed to dwindling diversities of tree species
available as a substrate (Murphy and Lugo 1986).
Lichens inhabit all terrestrial habitats of the Earth,
yet they are among the most underexplored groups of
living organisms. The majority of the biodiversity and
conservation efforts put greater emphasis on “charismatic
species,” leaving a challenge to develop effective
conservation and protection strategies for these less-
known and studied groups (Nascimbene et al. 2013;
Gheza et al. 2020).
Lichens play an important ecological role in their native
habitats and are sensitive to changes in moisture and air
pollution; hence, monitoring the populations can help
scientists track the effects of climate change and air quality
on ecosystems (Bates 2002; Nimis et al. 2002). In addition,
they also provide a wide range of microhabitats for insects
– including shelter, camouflage as survival strategies, and
insulation (Haines and Renwick 2009; Fang et al. 2020).
Moreover, it has been known to provide ethnobotanical
and pharmacological roles in traditional medicine systems
around the world (Agelet and Vallès 2003; Azuelo et al.
2011; Chandra et al. 2017; Yang et al. 2021). Thus, well-
deserved attention is important not just for maintaining
biodiversity and ecosystem function but for conservation
for both cultural and medical reasons as well.
Among the mountain ecosystems in the central region of
Mindanao Island is Mt. Musuan, which is surrounded by
remains of forest and cultivated agricultural areas near
Valencia City and is considerably rich in fauna and flora
assemblages (Amoroso et al. 2002). However, increased
human-induced interventions in the nearby areas and
climate change pose threats to the already dwindling flora,
fauna, and fungi. With the help of afforestation initiatives
nearly 20 years ago, various trees have emerged, which
– through time – have created a favorable microclimatic
condition, paving the opportunity for other tree species
to thrive (Aribal et al. 2015) and, consequently, bark-
dwelling lichens.
To date, comparatively little attention has been given to
the species composition of lichen fungi along a lowland
secondary forest ecosystem in the Philippines; hence, this
study was undertaken.
MATERIALS AND METHODS
Study Site
The study was conducted in Mount Musuan at Maramag
in the province of Bukidnon in Central Mindanao. This
site is an isolated, low grass-covered andesitic lava dome
and tuff cone that rises to 646 meters above sea level (masl
onward) above flat farmland. It has a total land area of 425
ha, with 169 of those being both natural and plantation
forests (Paquit et al. 2023). Its climatic data recorded with
air temperature ranges from 25–27 °C with an average
of 26 °C plus a relative humidity of 70–85% (80%). The
soil temperature (5-cm depth) is 25–26 °C (–28°C) with
an annual rainfall of 150–250 mm (190 mm on average)
(Azuelo et al. 2020).
Prior to the conduct of the study, a field reconnaissance
survey was carried out to verify the presence of lichen
species in different land use types. The different land use
types were identified based on the Mt. Musuan resource
map (Figure 1) developed by Paquit et al. (2023). These
land use types were: [a] LTER plot (350 masl); [b]
Thailand acacia plantation (TAP; 405-450 masl); [c]
mixed species forest (MSF; 455–500 masl); [d] grass-
shrubland (505–550 masl); [e] teak forest (TF; 530–545
masl); [f] Pinus caribaea plantation (PP; 555–600 masl);
and [g] built-up peak/summit (BUP; 605+ masl). A GPS
(global positioning system) was used to generate spatial
information such as the altitude and coordinates of each
identified land use type.
Collection of Lichen Samples
An inventory of lichen species was conducted from
March–April 2023 across identified land use types of
Mt. Musuan (Figure 2) using a series of transect walks.
In each land use type, an opportunistic sampling method
was employed to record all the lichen species. Specific
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microhabitats limited to fallen logs, trunks of trees and
shrubs (at 200 cm from the ground level), and soils were
searched. Only corticolous and terricolous lichens were
assessed.
Collected specimens were placed in individual bags and
properly labeled with detailed information for further
examination in the laboratory. Voucher specimens were
dried and deposited in Central Mindanao University
Herbarium (CMUH) in Bukidnon, Philippines.
Lichen Identification
Morpho-anatomical characters were examined using
a stereoscope and an optical microscope together with
available dichotomous taxonomic keys from various
scientific articles and journals. The following studies
were the most routinely used: Wolseley and Aguirre-
Hudson (1995; for macrolichens), Lücking et al. (2009),
Rivas Plata et al. (2011; for Graphis and Graphidaceae),
Schumm and Aptroot (2012; for general tropical lichens
Figure 1. Map of Mt. Musuan, Bukidnon, southern Philippines: [A] map of Mindanao Island; [B] Mt. Musuan resource map adopted from
Paquit et al. (2023).
Figure 2. Different identified land use types of Mt. Musuan, Bukidnon, southern Philippines: [a] LTER plot; [b] teak forest; [c] Thailand
acacia plantation; [d] mixed species forest; [e] grass-shrubland; [f] Pinus caribaea plantation; [g] built-up peak/summit.
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from Southeast Asia), and Aptroot (2021; Pyrenulaceae
and Trypetheliaceae). We also consulted Paguirigan et al.
(2020) to confirm citations and records in the most current
checklist of Philippine lichens. Subsequently, identified
specimens were referred to experts for verification.
Data Analysis
Descriptive statistics such as graphs and seriation analysis
to visualize the distribution of lichen fungi across land
use types were generated using PAST (Palaeontological
Statistics Software).
RESULTS
Species Composition across Land Use Types
An initial field inventory of the lichen diversity in Mt.
Musuan identified a total of 38 species distributed in
26 genera and 14 families. Notably, two lichen species
were revealed as new records for the Philippines, viz.
Letrouitia subvulpina and Pyrenula globifera (Figure
3). The majority (63%) of the collected specimens
were microlichens, characterized morphologically with
crustose thalli formations, whereas only 37% were
macrolichens. Further results portrayed Graphidaceae as
the most represented family with 10 species – followed by
Caliciaceae (6 spp.), Physciaceae (3 spp.), Parmeliaceae
(3 spp.), and Arthoniaceae (3 spp.) (Table 1).
New Records in the Philippines
Letrouitia subvulpina (Nyl.) Hafellner
Specimen examined. PHILIPPINES: Mt. Musuan,
Maramag, Bukidnon, Philippines, 443 masl, 7º52’48” N
125º03’53” E, on the bark of Koompassia excelsa, 14 Mar
2023; ECT50 (CMUH).
Habitat and geographical distribution. Bark of tropical
forests; Cambodia and Nepal (Shi et al. 2015), Sri Lanka,
Indonesia, Africa, Caribbean Islands, South America,
Australia, Pacific Islands (Hafellner 1983), and new to
the Philippines.
Figure 3. Habit and ascospores of lichen species recorded as new
to the Philippines: [a and b] Letrouitia subvulpina; [c and
d] Pyrenula globifera.
Table 1. List of lichen species found in Mt. Musuan.
Macrolichens
Class, Order Family Scientic name
Lecanoromycetes
Lecanorales
Parmeliaceae Parmelinopsis minarum (Vain.) Elix & Hale
Parmotrema cristiferum (Taylor) Hale
P. tinctorum (Despr. ex Nyl.) Hale
Lecanoromycetes
Caliciales
Caliciaceae Dirinaria applanata (Fée) D.D. Awasthi
D. picta (Sw.) Clem. & Shear
Pyxine petricola Nyl.
Pyxine sp.
Physciaceae Heterodermia obscurata (Nyl.) Trevis.
H. propagulifera (Vain.) J.P. Dey
H. speciosa (Wulfen) Trevis.
Lecanoromycetes
Peltigerales
Pannariaceae Physma byrsaeum (Afzel. ex Ach.) Tuck.
Coccocarpiaceae Coccocarpia epiphylla (Fée) Kremp.
Collemataceae Leptogium cyanescens (Ach.) Körb.
L. moluccanum (Pers.) Vain.
Microlichens
Class, Order
Family Scientic name
Dothideomycetes
Trypetheliales
Trypetheliaceae Astrothelium sp.
Bogoriella decipiens (Müll. Arg.) Aptroot & Lücking
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Remarks. The ascospores information is similar to
L. vulpina, L. muralis, and L. sayeri, with stair-type
ascospores, sometimes muriform with 2–4 spores per
ascus (Dombrowski 2022).
Pyrenula globifera (Eschw.) Aptroot
Specimen examined. PHILIPPINES: Mt. Musuan,
Maramag, Bukidnon, Philippines, 473 masl, 7º52’49” N
125º03’60” E, on the bark of Glochidion album, 14 Mar
2023; ECT72 (CMUH).
Habitat and geographical distribution. Pantropical
(Aptroot 2021); new to the Philippines.
Remarks. This pantropical species produces asci
containing two muriform ascospores (Aptroot and Cáceres
2013); moreover, it has an inspersed hamathecium and
UV-thallus due to the absence of lichexanthone (Aptroot
2021).
Distribution of Lichen Species across Land Use Types
Among the land use types of Mt. Musuan, MSF harbors
most of the lichen individuals (Figure 4). As a result, a
high proportion of species were recorded in MSF, which
comprises 22 out of 38 lichen species – followed by
TF, BUP, and LTER plot with 15, 14, and 11 species,
respectively. The remaining land use types which host
fewer species were grass-shrubland (10), PP (8), and TAP
(6) (Figure 4A).
Seriation analysis highlights the occurrence of lichen
species across land use types (Figure 4C). Among the
lichen species, Cryptothecia spp. of Arthoniaceae were
widely distributed, which spans across land use types.
In addition, nine lichen species were broadly distributed,
found to be observed at more than three land use types.
Meanwhile, 17 lichen species documented in this study
exhibited restricted distribution, which was found to
be present only in one land use type, viz. Letrouitia
subvulpina and Phaeographis sp. recorded exclusively
in TF, Astrothelium sp. in LTER plot, Bacidia sp., and
Septotrapelia triseptata in grass-shrubland. Among the
land use types, MSF houses the most numbered rare
lichens with nine species, followed by BUP with three
rare species.
DISCUSSION
Findings in the current study suggest that lichen species
richness in Mt. Musuan is closely related to the availability
of various tree species combined with canopy openness.
This observation was depicted in MSF, which houses the
richest species composition. Although characterized as one
Lecanoromycetes
Ostropales
Graphidaceae Allographa sp.
Diorygma sp.
Dyplolabia afzelii (Ach.) A. Massal.
Glyphis cicatricosa Ach.
Glyphis sp.
Graphis sp. 1
Graphis sp. 2
Phaeographis glyphiza (Nyl.) Zahlbr.
Phaeographis sp.
Sarcographa labyrinthica (Ach.) Müll. Arg.
Lecanoromycetes
Caliciales
Caliciaceae Calicium sp.
Stigmatochroma sp.
Lecanoromycetes
Lecanorales
Byssolomataceae Septotrapelia triseptata (Hepp) Aptroot
Lecanoraceae Lecanora tropica Zahlbr.
Ramalinaceae Bacidia sp.
Lecanoromycetes
Teloschistales
Letrouitiaceae Letrouitia domingensis (Pers.) Hafellner & Bellem.
●L. subvulpina (Nyl.) Hafellner
Arthoniomycetes
Arthoniales
Arthoniaceae Arthonia sp.
Cryptothecia sp. 1
Cryptothecia sp. 2
Eurotiomycetes
Pyrenulales
Pyrenulaceae ●Pyrenula globifera (Eschw.) Aptroot
P. quassiicola Fée
Note: (●) indicates new records in the Philippines
Table 1. Cont.
Microlichens
Class, Order Family Scientic name
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of the plantation forests, several tree species have emerged
successfully in the area. These include Rhus tritenensis,
Breyna vitis-idea, Koompassia excelsa, Neonauclea
media, and Wikstroemia lanceolata with a mean stem
density of 5333/ha and a mean diameter at breast height
(DBH ± SE) of 8.14 ± 0.35 cm (Paquit et al. 2023). Such
trees possessed variable traits, including bark type and
texture, which provided vast substrate options to host
corticolous (bark-dwelling) foliose and crustose lichen
species in the area. No fruticose species was found in the
surveyed sites. In addition to the availability of various
tree species, MSF also possessed open canopy densities,
allowing the lichens to receive a greater proportion of the
sunlight available for food production.
Figure 4. Lichen species across land use types: [A] species richness; [B] number of individuals; [C] kinds of species across land use types.
Note: [TF] teak forest; [TAP] Thailand acacia plantation; [MSF] mixed species forest; [GS] grass-shrubland; [PP] Pinus caribaea
plantation; [BUP] built-up peak/summit
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Conversely, the occurrence of lichen species decreased
in the LTER plot. This land use type was part of the
natural forest patch of Mt. Musuan with dense canopy
cover and relatively dominated by understory vegetation
– specifically, Calamus sp. This confirms the positive
influence of various tree species and canopy openness
on lichens, similar to the findings of Benítez et al.
(2019), who reported that the richness of lichen species
composition highly depends on tree species richness
and canopy openness. The observed relationship was
consistent with other land use types. For instance, lichen
species composition decreased gradually in abundance
with land use types dominated by single tree species
such as in TAP and PP. Similarly, the TF dominated by
plantations of Tectona grandis and BUP with Gmelina
arborea also revealed a decline in lichen species
composition. However, the forest stand in TAP and PP
displays high canopy cover and branch density, which
could be one of the reasons why these areas hosted the
fewest lichen species. This microenvironmental condition
is considered suboptimal for the growth of many lichen
species because it traps more humidity, which encourages
greater competition for bryophytes (Bäcklund et al. 2016).
Among the land use types, grass-shrubland was the only
area dominated primarily by Imperata cylindrica. This
dry land type served as the preferred microhabitat for
Septotrapelia triseptata and Bacidia sp., colonizing the
exposed slope of the area and growing directly over the
soil (terricolous lichens). A study by Sipman et al. (2013)
also observed growths of such species on the slope of Mt.
Mantalingahan, Palawan, within 300 masl. In high-altitude
grassland, terricolous lichens have been considered as
indicators of human-induced disturbances (Rai et al.
2011). Considering the abundance of Septotrapelia
triseptata and Bacidia sp. in the area, these can be
potential indicator species of dry tropical grassland since
they can only be found thriving and colonizing such areas.
A total of 38 lichen species were distinguished in Mt.
Musuan, which is few compared to other tropical forest
ecosystems worldwide. More than half of the recorded
species are restricted to a single land use type. The
observed restricted distribution could be attributed to
variations in the available potential substrates across
different land use types. As noted, lichens thrive in
specific ecological conditions and microsites provided
by host trees (Cordero-S et al. 2021; Enquist et al. 2019;
Bartels and Chen 2012), which supports the disparity in
abundance and distribution.
The majority of the lichen species identified in Mt.
Musuan are crustose, i.e. crust-like and tightly attached
to their substrate. These types of lichens are generally
overlooked in similar studies (Barajas-Morales and
Jimenez 1990); nevertheless, they have been considered
the most diverse and abundant growth form, contributing
significant biomass in a tropical dry forest (Miranda-
González and McCune 2020).
Due to their unique poikilohydric nature, lichens are
susceptible to periodic desiccation, making these
organisms sensitive to both natural and anthropogenic
disturbances (Chuquimarca et al. 2019). The history
of habitat conversion has intensified Mt. Musuan’s dry
climatic conditions, resulting in low species richness of
foliose lichens. In response to such conditions, foliose
lichens evolved to acquire thalli with a narrow surface
area such as those in Caliciaceae and Physciaceae, which
minimizes the evaporative loss. More importantly, Mt.
Musuan was surrounded by cultivated areas and open
degraded sites, which may explain the absence of fruticose
lichens – the most sensitive group of lichens (Fenton 1960;
Blum 1973). Several studies conducted in habitats with
extreme environmental pressures have also confirmed that
crustose and foliose growth forms were the most adaptive
(Zulkifly et al. 2011; Bawingan 2014). Indeed, simpler
thallus morphology forces lichens to minimize demands
for nutrient accumulation, limit water loss (Armstrong
2017; McCune 2000), and ultimately be able to withstand
varying environmental constraints. Among the frequently
observed crustose lichens were Cryptothecia spp. The
commonness of these species across land use types was
primarily due to the fact that Mt. Musuan was already
a pronounced disturbed habitat. This observation was
consistent with the findings of Thüs et al. (2021), who
reported that the significant presence of these species
and other sterile crustose taxa serves as an indicator of a
disturbed forest plot.
Nonetheless, two species were considered as new
records in the Philippines, viz. Letrouitia subvulpina and
Pyrenula globifera. This underlines the importance of
comparative attention to secondary forest ecosystems as
their habitat types have the potential for discovering more
taxa to be added to the Philippine lichen checklist. More
importantly, this would encourage effective management
and biodiversity conservation efforts of various land use
types, as lichens are sensitive to anthropogenic threats and
pressures from environmental conditions.
ACKNOWLEDGMENTS
The authors would like to express their heartfelt gratitude
to the following: Dr. André Aptroot for the verification
of several crustose lichen species; Central Mindanao
University and the Center for Biodiversity Research and
Extension in Mindanao for their unwavering support; the
Commission on Higher Education for funding the research
project titled “Biodiversity Conservation and Utilization
Philippine Journal of Science
Vol. 152 No. 6A, December 2023
Taer et al.: Lichens of Mt. Musuan, Bukidnon,
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of Products for Long-term Ecological Research Sites”;
and Surigao del Norte State University Mainit Campus for
granting permission to access their microscopy materials.
ECT would like to thank DOST Project STRAND for
the scholarship grant. In addition, MDF would like
to acknowledge funding from the National Science
Foundation (NSF-DEB 1754697 and 1754667).
DECLARATION OF COMPETING
INTEREST
The authors declare that they have no known competing
financial interests or personal relationships that could have
appeared to influence the work reported in this article.
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