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B IOD I V E R S I TA S ISSN: 1412-033X

Volume 21, Number 4, April 2020 E-ISSN: 2085-4722


Pages: 1597-1613 DOI: 10.13057/biodiv/d210441

Review:
Biodiversity of forests over limestone in Southeast Asia with emphasis
on the Philippines

PAUL JOHN S. TOLENTINO1,, JOHN RYAN L. NAVIDAD1, MARJORIE DELOS ANGELES2,


DESAMARIE ANTONETTE P. FERNANDEZ3, ELAINE LOREEN C. VILLANUEVA4,
REN DIVIEN R. OBEÑA1, INOCENCIO E. BUOT, JR.2
1University Research Associate I of CONserve-KAIGANGAN Program Project 1, Institute of Biological Sciences, College of Arts and Sciences,

University of the Philippines Los Baños. College, Batong Malake, Laguna 4031, Philippines. Tel.: +63-2-536-2807, email: [email protected]
2Plant Biology Division, Institute of Biological Sciences, College of Arts and Sciences, University of the Philippines Los Baños. College, Batong

Malake, Laguna 4031, Philippines


3Animal Biology Division, Institute of Biological Sciences, College of Arts and Sciences, University of the Philippines Los Baños. College, Batong

Malake, Laguna 4031, Philippines


4Institute of Biological Sciences, College of Arts and Sciences, University of the Philippines Los Baños. College, Batong Malake, Laguna 4031, Philippines

Manuscript received: 3 September 2019. Revision accepted: 23 March 2020.

Abstract. Tolentino PJS, Navidad JRL, Angeles MD, Fernandez AP, Villanueva ELC, Obena RDR, Buot Jr IE. 2020. Review:
Biodiversity of forests over limestone in Southeast Asia with emphasis on the Philippines. Biodiversitas 21: 1597-1613. A
comprehensive review of literature was carried out to determine the status of plant and animal diversity on forests over lime stone in
Southeast Asia (SEA), particularly in the Philippines. Angiosperm records are available in Peninsular Malaysia (1216 spp.); West Java
and Seram Indonesia (101 and 149 spp., respectively); Laos (135 spp.); Thailand and Myanmar (1 sp.); and Limestone areas in Vietnam.
Pteridophytes were recorded in Malaysia (32 spp.) while Bryophytes are recorded in Peninsular Malaysia (59 spp.). In the Philippines,
there are plant records in: Masbate (61 spp.); Isabela (169 spp. Pteridophytes); Bohol (12 spp.), and Samar forests over limestone (29
spp. palms and 20 spp. orchids). A floral assessment in Samar Island Natural Park (SINP) includes species (212 spp.) that can possibly
be found but are not limited to karsts. New Philippine endemic species are also recorded in Cebu, Palawan, and Panay Island. There are
animal records in SEA including Vietnam (Bats-36, Bird-1, and Langurs-5 spp.); Malaysia (Sciuridae-1, Bats-28, Birds-129, Reptiles-
17, and Invertebrates-74 spp.); Thailand (Murids-12, Reptiles-11, and Amphibian-1 sp.); and Myanmar (Reptiles-15 spp.). Records in
the Philippines include: Mammals (Bicol-9, Mt. Irid-24, Mt. Aruyan-1, and Cebu-1 species), and; Birds (Cebu-1 sp.). A terrestrial faunal
assessment in SINP includes species (182 spp.) that can possibly be found but are not limited to karsts. Forests over limestone are still
largely understudied and the potential of discovering species is high. Further research is critical to establish science-based initiatives and
policies that will protect and conserve limestone ecosystem biodiversity while allowing the utilization of its biological resources at a
sustainable level.

Keywords: Biodiversity potentials, conservation, flora and fauna, karst, Southeast Asia

INTRODUCTION 10% of the total land area in Southeast Asia (Day and
Urich 2000) with the most extensive found in Vietnam,
Forest over limestone is a type of forest formation that Thailand, Indonesia, and Malaysia (Fernando et al. 2008).
can be found within tropical rainforest regions along with The Philippines is recorded to also possess extensive forest
limestone hill areas. Limestone dissolution and abundance over limestone landscapes. While 30,000 km2 of the
of calcium in the soil contributes to strongly irregular country’s land area are karst landscapes, a large portion of
geomorphology referred to as "karsts". Limestone this is still unknown to science because of the low priority
landscapes, though generally perceived to be lower in and limited research support of the government.
stature than other forest types, are known worldwide as Recognizing the importance of limestone ecosystems as a
areas of great biological importance (Struebig et al. 2009) host of unique flora and fauna, a strategic action plan is
because of its rich endemic flora and fauna (Fernando et needed to save and sustainably manage the country’s
al. 2008). It is also significant in terms of its mineral and unique ecosystem (BMB-DENR 2019).
aquifer resources, aesthetic, cultural, and tourism value. The need for research on forest over limestone has been
Southeast Asia comprises 11 countries, namely: identified as a conservation priority for the sustainability of
Myanmar, Vietnam, Laos, Thailand, Cambodia, Malaysia, these forests especially that natural and anthropogenic
Singapore, Indonesia, Brunei, Philippines and East Timor disturbances are increasing (Sodhi et al. 2010). As an
(Sodhi et al. 2004). The region has abundant large example, unsustainable use of resources can change the
formations of limestone landscapes, which cover an area of soil's quality and dynamics thus altering the forest's
460,000 square kilometers (km2) and accounts for about productivity and affecting its species composition. Given
1598 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

the fragile nature of limestone forests, there is a need for BIODIVERSITY OF FOREST OVER LIMESTONE
practical methods for the extraction of raw materials that LANDSCAPES
are more compatible with the conservation of biodiversity
in limestone areas. Research is a crucial factor to consider Preliminary studies indicate that the Philippine karst
before doing anything that will cause change to limestone landscapes have a total area of 35 000 km² (Figure 1)
landscapes. Despite the significance and high potential of which is about 11.7% of the country’s total land area
discovering new scientific breakthroughs, biological data (BMB-DENR 2019) and about 29% is protected by law
focusing on forest over limestone is still lacking. It is a (Wagner 2013). However, there are no existing legislation
perfect opportunity to study forests over limestone and gain that directly addressed the protection and conservation of
more knowledge of its biological information. Researches karst areas in the country, and its protection is mainly
on forest over limestone focusing on its high biological indirect. Significant actions for the protection of karst in
importance should be urgently considered in order to the Philippines only address specific aspects, such as the
protect its biodiversity. Thus, threats on forest over National Caves and Cave Resources Management and
limestone could be minimized by implementing research- Protection Act in 2001 and the inclusion of karst water
based knowledge on proper management practices, land resources in the country’s National Action Plan (NAP)
use plans, and conservation strategies toward a sustainable under the United Nations Convention to Combat
ecosystem. Desertification (UNCCD) (Restificar et al. 2006). Tourism
This study assessed the status and the biodiversity of is one of the driving factors for karst conservation and
forests over limestone in Southeast Asia, with emphasis on some portion of karst areas are protected only because it is
the Philippine setting. Based on several literature reviews, part of a larger protected landscape such as nature reserves,
it also determined the biodiversity found in forests over natural parks, wildlife sanctuary, or protected seascapes.
limestone and provided an assessment of its potentials. The government shoulders a big responsibility in
Lastly, this article evaluated the conservation efforts recognizing the importance of protecting forests over
towards forests over limestone in Southeast Asia. limestone and its components which offer economic,
scientific, recreational and aesthetic resources. Given these,
they are also potentially highly sensitive so careful
DATA SOURCES protective management is essential (Watson et al. 1997).
The karst areas in the country (Figure 2) vary in terms
A comprehensive review of several published literature of form and age but most of it formed in Tertiary and
regarding biodiversity, potentials, and conservation efforts Quaternary carbonates (Fernando 2008). According to
in forests over limestone of Southeast Asia was employed BMB-DENR (2019), the dominant limestone formations in
and compared with the Philippine setting. Reputable the Philippines are karst towers and cones. It is also
scientific journals were among the sources of information characterized by caves, sinkholes, and aquifers. One of the
such as Trends in Ecology and Evolution, BioScience, most extensive recorded is the Calbiga Karst on Samar
Conservation Biology, Biological Conservation, Island with many other significant karst areas found on
Biodiversity and Conservation, Cave and Karst Science, other large islands. Important karst areas are also found in
Journal of Threatened Taxa, and Acta Carsologica. Several Luzon (Cagayan, Kalinga-Apayao, Ilocos and Bicol
published journal articles about tropical forests over regions), Visayas (Bohol and Cebu) (Cadiz and Buot 2010,
limestone in Southeast Asia were also consulted. 2011; Lillo et al. 2020), and Mindanao (Negros, Davao and
Descriptions of the forest over limestone and its Cotabato) (Restificar et al. 2006). Pinnacle karsts and
composition in the different regions of the Philippines was conspicuous steep-sided karst towers are found in northern
reviewed from Fernando et al. (2008) and Restificar et al. Palawan-specifically Coron Island-and Palawan’s west
(2006). The threats which include limestone quarrying, coast (Fernando et al. 2008). Bohol island, on the other
land use change, deforestation, hunting, illegal logging, and hand, is dominated by dome-shaped karst hills and
habitat degradation of forests over limestone were in numerous sinkholes, dry valleys, karst fields, and caves
reference to the Cave Management, Protection and (Restificar et al. 2006).
Conservation Strategy and Action Plan (2019-2028) of Samar Island Natural Park (SINP) covers an area of
BMB-DENR (2019), Woxvold et al. (2009), and Clements about 333,300 hectares. The interior natural habitats of
et al. (2006). In addition, the guidelines for forest over Samar Island are dominated by lowland evergreen
limestone protection were consulted with the publications rainforests and limestone forests (UNDP 2007; Taylor et al.
from Restificar et al. (2006) and Watson et al. (1997) 2015). It was declared as a protected area under the NIPAS
guidelines for cave and karst protection. The animal Act in 2003. The area is worthy of attention as it holds a
species mentioned were verified based on the latest significant portion of karst landscapes including the
assessments by the International Union for Conservation of Calbiga karst which is one of the largest limestone areas in
Nature (IUCN). Lastly, each listed species of plants was the country which covers an area of about 900 km 2. The
verified through The International Plant Name Index Calbiga Cave Protected Landscape found within the
(IPNI). Calbiga karst contains 12 caves, with the five-kilometer-
long Langun-Gobingob System being the largest (Restificar
et al. 2006).
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1599

Karst landscapes provide protection and safety to microclimate in karst areas (Hamilton-Smith 2001).
numerous species (BMB-DENR 2019; Clements et al. Limestone’s unique characteristics such as its chemistry,
2006) in which the surface vegetation is often distinctive hydrology, geology, and micro-climates, is a driving factor
and supports a wide range of karst-endemic species of in the evolution of its biological components in order to
plants, vertebrates, and invertebrates (Hamilton-Smith adapt to their environment including some species of plants
2001). Southeast Asia’s karsts support a very high level of (orchids), vertebrates (bats, fish), and invertebrates (snails,
endemic species (Clements et al. 2006; Latinne et al. 2011; beetles) (BirdLife/FFI/IUCN/WWF 2014). The limestone
Schilthuizen et al. 2005) and is considered as one of the species are adapted with the highly alkaline environment
most biologically rich regions in the world (Sodhi et al. and plants are also able to cope with the extreme water
2004). Most karsts are scattered and isolated as small shortage in the soil during drought seasons of the year (FFI
limestone hills (Schilthuizen et al. 2005; Clements et al. 2001). Moreover, many limestone species provide
2006; Struebig et al. 2009) and there is a high degree of important ecosystem services (BirdLife/FFI/IUCN/WWF
localized endemism, due at least in part to the diversity of 2014).

Figure 1. Karst areas in the Philippines shaded in black (based on Balázs 1973; Restificar et al. 2006)
1600 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

A B

Figure 2. Karst formations in the Philippines: A. Taraw Cliff, El Nido, Palawan (Photograph by J.R. Navidad), and B. Karst near Linao
Cave, Guiuan, Eastern Samar (Photograph by P.J. Tolentino)

A B

Figure 3. A. Short stunted plants on exposed vertical cliffs; B. Tall trees on gentler areas of Paranas, SINP. Photographs by P.J.
Tolentino.

Sadly, karst outcrops are under immense pressure from intricate terrains that can be found within the limestone
mining interests, local harvest of animal resources (e.g., landscapes result in high species diversity of the area
guano, bird's nest-used for nido soup), land conversion, (Asanok and Marod 2016; Clements et al. 2006; Saw et al.
illegal hunting/poaching, and over-extraction of timber 2010). The surface rock layer of limestone landscapes has
products (Clements et al. 2006; Struebig et al. 2009). The innumerable perforations and hollow areas that allow
SEA region is recognized as a biodiversity hotspot because rainwater to drain fast underground. The upper rock layer,
its rich flora and fauna is threatened by activities such as for the most part, holds a thin substrate of soil that cannot
rapid land-use change and other anthropogenic activities, provide for a plant's sustenance alone. High temperatures
putting much of the biodiversity at risk for extinction. and exposure also require plants to have strategies for
surviving acute drought (FFI 2001). For this reason, most
Flora of forest over limestone of the plant species found on forests over limestone are
The forest over limestone typically has greatly varying deciduous which is part of their adaptation to seasonal
tree heights when compared to other forest types depending shortages in water.
on the site and physical habitat, from short stunted trees on The presence of many narrow endemic species or those
exposed vertical cliffs to tall trees (Figure 3) up to 35 that only exist in one area can command thousands of
meters (m) tall on gentle hills (Fernando et al. 2008). dollars per plant when traded on the illegal market; e.g.
Limestone landscapes are comprised of several diverse slipper orchids (Paphiopedilum spp.). Notable cycads
plant communities and are floristically unique compared to (primitive, palm-like trees) and fan palms that can recover
other forest types. The varied ecological niches and even after severe wilting are also present in limestone
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1601

ecosystems (FFI 2001). The interest in this component of (2008). Species belonging to Rubiaceae are also be found
the biota is growing rapidly, partly because a range of in forests over limestone of Eastern Samar, Visayas based
particularly exotic and often attractive plants, such as on a checklist by Ordas et al. (2018). Lastly, a floral
orchids, begonias (Peng et al. 2015, 2017; Phutthai and diversity assessment in Samar Island Natural Park by
Hughes 2017) and pitcher plants are included in karst flora Quimio (2016) recorded a total of 212 timber species
(Hamilton-Smith 2001). The unusual soil condition paved where 86% of individual trees were dipterocarps, in 14
the way for the high environmental heterogeneity found species, with Shorea squamata Benth. & Hook.f. and
within forests over limestone (Pérez-García et al. 2009). Shorea polysperma Merr. being the most frequent. SINP is
The vegetation of a limestone forest is also greatly varied located where the sedimentary formation generally consists
depending on the site's prevailing conditions. Many of of basement rocks, sometimes with overlying clastic rocks
these are calcicoles, species which are adapted to grow on or limestone.
limestone soils (Clements et al. 2006). The high floral richness that has been recorded on forest
In a study on the tower karst limestone formation in over limestone are still underestimated (Clements et al.
Selangor, Malaysia (Kiew 2014), a total of 269 species of 2006) and lot of biological data could still be unveiled.
vascular plants were recorded of which 51 are endemic and Exploring the remote areas of forest over limestone could
80 are calciphiles. Some of the most common families lead to the discovery of new plant species of economic
listed in the study were Orchidaceae (23 species), importance. A table showing the compiled number of
Apocynaceae (20 species), Rubiaceae (14 species), Araceae species found in forests over limestone of Southeast Asia
(12 species), Gesneriaceae, Moraceae (9 species), and from different floral studies is shown in Table 1.
Urticaceae (9 species). Among these families, Ficus
(Moraceae) comprise the largest genus. In the limestone Fauna of forest over limestone
forest of Seram Island in Indonesia (Ranlund 2011), a total The distinctive vegetation together with the often highly
number of 149 species were recorded. The two most dissected terrain of karst leads in turn to an especially
abundant species in Seram Island are Aglaia sapindina attractive environment for unique species of invertebrates,
Harms. and Myristica lancifolia Poir. Other abundant reptiles, birds and mammals. In fact, some species appear
species include Alangium javanicum (Blume) Wangerin., to be fully confined to karst regions (Hamilton-Ssmith
Gymnacranthera paniculata Warb., Celtis philippinensis 2001). By far, lizards under the Family Gekkonidae are the
Blanco., Chisocheton ceramicus Miq., and Palaquium most well-represented taxa among forest over limestone
amboinense Burck. biodiversity studies in Southeast Asia. On a study by
In the Philippines, only a few studies focusing on Grismer et al. (2018), 12 new karst-adapted gekkonid
limestone forests have been conducted. The existing studies species under the genus Cyrtodactylus were recorded from
on plant diversity which includes forest over limestone isolated limestone ecosystems in east-central and southern
showed varying results in different regions. In Baladingan, Myanmar. These geckoes have evolved specialized
Ticao Island, 61 species in 32 families were recorded, of scansors under their feet that allow them to stick to surfaces
which 23 species are endemic and approximately half of such as limestone. Newly discovered species have been and
the 23 species are island endemics (Calumpong 2014). In are continuously being described from Laos (Luu et al.
Palawan near St. Paul’s Bay, the common species dominant 2016ab, 2017; Nazarov et al. 2018; Schneider et al. 2011,
in the forest over limestone includes Vitex parviflora Juss., 2014), Indonesia (Grismer et al. 2014; Riyanto et al.
Afzelia rhomboidea Fern.-Vill., Sindora supa Merr., Intsia 2014), Malaysia (Grismer and Onn 2009, 2010; Grismer et
bijuga Kuntze., Albizia acle Merr., Wallaceodendron al. 2008a,b; Grismer et al. 2013, 2014a,b,c, 2016; Wood et
celebicum Koord., Pterocarpus indicus Willd., al. 2013), Myanmar (Connette et al. 2017; Grismer et al.
Kingiodendron alternifolium Merr. & Rolfe., Wrightia 2018a,b), Thailand (Ellis and Pauwels 2012; Grismer et al.
pubescens R.Br. (Fernando et al. 2008). In the case of 2008, 2014; Panitvong et al. 2012; Pauwels and Sumontha
Dinagat Island, where the forest over limestone is on 2014; Wood et al. 2017), and Vietnam (Ngo 2011; Nguyen
mountainous topography, tree species like Terminalia et al. 2017; Quang et al. 2007; Rösler et al. 2005; Ziegler et
catappa L., Barringtonia asiatica Kurz., Hernandia al. 2008). A new species of sticky frog, Kalophrynus
nymphaeifolia (C.Presl) Kubitzki., Barringtonia racemosa calciphilus, found only in the karst hills and mountains of
(L.) Spreng., Talipariti tiliaceum (L.) Fryxell., and Melinau Limestone Formation, Malaysian Borneo, has also
Millettia pinnata (L.) Panigrahi. are dominant (Lillo et al. been recently discovered (Dehling 2011). Another notable
2019). Many herbs are also documented in the crevices of species of frog, Ansonia khaochangensis sp. Nov., from
karst limestone areas of the Philippines including the southern Thailand is the first of its species that prefer to
species belonging to Araceae, Begoniaceae, Gesneriaceae, live in a karst ecosystem as compared to all other Ansonia
Orchidaceae (Fernando et al 2008). Fern and fern allies are species that are adapted to a lotic lifestyle. This emphasizes
also found within this forest type of Palanan, Isabela where that aside from promoting evolution of new species, karst
Barcelona et al. (2006) recorded a total of 169 species. ecosystems also play a part in the evolution of remarkably
Twelve species of dipterocarps were recorded in the different lifestyles (Grismer et al. 2017).
aseasonal southern part of Bohol Island by Fernando et al.
1602 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

Table 1. Major plant groups and the number of species found in different forests over limestone of Southeast Asia based from recent
floral surveys

Major plant No. of


Location Notes Reference
group species
Spermatophytes
Angiosperms 1216 Peninsular Malaysia limestone 21% endemics; 11% calciphiles (strictly Adam and Mamat (2005);
flora confined to karsts) Chin (1977); Clements
(2006); Kiew (2014);
Nizam et al. (2012)
42 Peninsular Malaysia 42 Gesneriaceae species; 28 are endemic Rahman and Kiew (2018)
and 16 are restricted to a single or adjacent
hill.
4 Peninsular Malaysia Impatiens (Balsaminaceae) species; 1 Kiew (2016)
widespread on karst limestone in Kelantan
and Pahang; 3 other new species narrowly
endemic to Kelantan limestone and are
critically endangered.
6 Peninsular Malaysia Microchirita (Gesneriaceae) restricted to Rafidah (2017)
limestone areas.
1 Peninsular Malaysia Exacum tenue (Gentianaceae); new record Rafidah (2018)
from Malaysia.
1 Relai Forest Reserve, Gua Vatica najibiana (Dipterocarpaceae); new Ummul-Nazrah et al.
Musang, Kelantan and Gua species (2018)
Tanggang, Merapoh, Pahang,
Peninsular Malaysia
3 Perak, Malaysia Three new species: Gymnostachyum Tan et al. (2014)
kanthanense Kiew (Acanthaceae), Meiogyne
kanthanensis (Annonaceae) and Vatica
kanthanensis (Dipterocarpaceae)
101 West Java, Indonesia Total of 38 families recorded for both sites. Satyani and Kusuma
(2010)
149 Lowland limestone forest on Ranlund (2011)
Seram Indonesia -
135 Limestone karst vegetation of Orchid species Kumar et al. (2016)
Vang Vieng District, Vientiane
Province, Laos
1 Thailand and Myanmar Begonia tenasserimensis sp. nov.; Endemic Phutthai and Hughes
to the hills of the Tenasserim Range. (2017)
6 Limestone areas in northern 6 new species of Begonia (Begoniaceae) Peng et al. (2015)
Vietnam
5 Xuan Son National Park, northern 3 restricted to limestone hills and 2 others Ngo and Holsher (2014)
Vietnam widely distributed.
20 Ba Be National Park, Vietnam 20 native tree species Binh et al. (2015)
29 Ben En National Park, Vietnam 26 most abundant tree species Nguyen et al. (2015)
1 Karst regions of China and Hemiboea crystallina, a new species of Chen et al. (2018)
Vietnam Gesneriaceae
260 Samar Island Natural Park Sites include but are not limited to forests Quimio (2016)
over limestone.
61 Baladingan, Ticao Island, 32 families; 23 endemics, half of which Calumpong (2014)
Philippines reported endemic only to Ticao; 9 species in
5 families are introduced; 10 species in 7
families are endangered.
19 General Philippine limestone 7 dominant leguminous trees; 9 other Fernando (2008)
dominant species; 3 smaller trees.
9 St Paul’s Bay, Palawan, 5 common species; other 4 frequent on
Philippines crevices.
9 Malapakan Island, Northern -
Palawan, Philippines
16 Aseasonal southern part of Bohol -
Island
1 Nug-as forest, Alcoy Lepeostegeres cebuensis (Loranthaceae); Pelser et al. (2016); Pelser
Municipality, southern Cebu New mistletoe species from Cebu, et al. (2011 onwards)
Philippines.
1 Cebu, Philippines Gymnosiphon philippinensis, new species of
Burmanniaceae
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1603

1 Limestone hills near El Nido, 1 new species of Amorphophallus (Araceae) Hetterscheid et al. (2012)
Palawan, Philippines
18 Northeastern Luzon near Palanan, - Co et al. (2006); Fernando
Isabela, Philippines 2008
29 Samar Island forests over 14 climbing palm species; 15 erect palm Adorador and Fernando
limestone species (2 new species: Pinanga (2019); Adorador and
(Arecaceae) (Adorador et al. 2020) and Fernando (2017);
Orania zheae (Oranieae, Arecoideae, Adorador et al. (2020)
Arecaceae) (Adorador and Fernando 2019)
20 Paranas and Marabut’s forest 20 orchid (Orchidaceae) species; 18 in Meneses et al. (2018);
over limestone in Samar Island, Paranas, 1 in Marabut, and 1 occurring in Meneses and Cootes
Philippines both. (2019)
3 Panay Island, Philippines 3 new species of Begonia sect. Baryandra Peng et al. (2017)
6 Across Visayas in the Philippines Rare tree species confined to limestone Peque and Holscher
areas. (2014)
2 Batu Caves tower karst 1 species usually found in limestone. Kiew (2014)
Gymnosperms formation, Malaysia

Pteridophytes 32 Batu Caves tower karst 1 endemic; 7 obligate calciphiles. Kiew (2014)
(ferns and fern formation, Malaysia
allies)
169 Bohol Island, Philippines 63 genera and 27 families; 21 species are Barcelona (2006)
Philippine endemics.
48 Samar Island Natural Park Sites include but are not limited to forests Quimio (2016)
over limestone.
10 Baladingan, Ticao Island, - Calumpong (2014)
Philippines
50 Forest over limestone in Cebu 15 families and 29 genera. Lillo (2020)
Island Key Biodiversity Areas

Bryophytes 59 Gunung Senyum Recreational 32 genera and 16 families of mosses. Norhazrina et al. (2019)
(mosses, liverworts Forest, Peninsular Malaysia
and hornworts)
- Southeast Asia See Mohamed and Tan (1998); Mohamed et Mohamed and Tan
al. (2005) (1998); Mohamed et al.
(2005); Clements (2006)

A B

Figure 4. Caves in Samar Island which are possible roosting sites for bats: A. Entrance of Linao Cave in Sulangan, Guiuan, Eastern
Samar; B. Saob cave in Basey, Samar. Photographs by P.J. Tolentino

Karst caves and outcrops in forests over limestone In an investigation by Furey et al. (2010) in the limestone
harbor a large percentage of bat populations, as these karst ecosystem of Vietnam, they recorded a total of 694
landscapes provide roosting resources and shelter for the bats representing 36 species and five families. This
vertebrates (Figure 4). This significant feature is often confirms that primary forests in Vietnamese karst are
neglected in conservation research (Struebig et al. 2009). critical for supporting large percentage of bat diversity in
1604 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

the country. In Indonesian Borneo, a study found 36 The limestone karsts of Southeast Asia are also home to
species of bats in the Sangkulirang limestone karst many small non-volant or non-flying mammals,
formations, including the karst associated Hipposideros particularly rodents of the Family Muridae. In a study of
larvatus, Rhinolophus creaghi and Rhinolophus pusillus 122 karsts in Thailand, 12 murid species were found
(Suyanto and Struebig 2007). including the karst-endemic Leopoldamys neilli and the
According to Kingston (2008), bats constitute about endangered limestone rat Niviventer hinpoon (Latinne et
30% of Southeast Asia’s mammal species and comprise al. 2013). The Laotian rock-rat Laonastes aenigmamus
about half of all mammal species in the tropical rainforest (Jenkins et al. 2005) and Paulina’s limestone rat
ecosystems, making it a critical component of the region’s Saxatilomys paulinae (Musser et al. 2005) are murids
threatened fauna. Even though there is paucity of data on discovered on the karsts of Laos, with S. paulinae being
Southeast Asian karst ecosystems on the comparative recently found to also occur in Vietnam (Nguyen et al.
studies of bats, Kingston (2008; 2003) pointed out that a 2015). The forest cover in limestone hills, while not
considerable number of bat species found only in Asia immune to deforestation, are still more resistant compared
depend upon intact forests for roosting and foraging. In to its surrounding areas making it a natural refuge to many
relation with this, it was also found that bat abundance, species endemic to the area (FFI 2001). The genus
species richness, and assemblage composition in Malaysia Trachypithecus is widely distributed in Southeast Asia with
is negatively affected by forest degradation and 6 species of limestone langurs (T. francoisi, T.
fragmentation (Furey et al. 2010; Struebig et al. 2008) which poliocephalus, T. delacouri, T. hatinhensis, T. laotum, T.
can also be implied to other Southeast Asian countries. ebenus) that occur in separate non-overlapping
Among avifauna, cave-nesting swiftlets also roost and geographical areas (Liu et al. 2019). Among larger
nest in caves of forests over limestone. A few species of mammals, the Laotian langur or Lao leaf monkey
swiftlets (genus Aerodramus) make nest from their Trachypithecus laotum is found only in Laos (Steinmetz et
hardened saliva. The edible saliva is a delicacy and is al. 2011), François’s langur Trachypithecus francoisi in
considered as one of the most expensive animal resources Southwestern China to northeastern Vietnam (Liu et al.
that humans consume (Thorburn 2015). The demand for 2019), Indochinese black langur T. ebenus in Laos and
authentic bird’s nest soup is mainly because of its Vietnam, while Delacour's langur Trachypithecus
perceived health benefits and not solely due to its taste delacouri, Hatinh langur T. hatinhensis, Cat Ba langur
(Marcone 2005). According to researchers from China and Trachypithecus poliocephalus poliocephalus, and the
Japan, the hardened saliva contains sialic acid-also found in critically endangered Tonkin snub-nosed monkey
human milk-which is thought to play a role in Rhinopithecus avunculus are found only in Vietnam (Dang
developmental advantages for breastfed infants and et al. 2019; Tuyet 2001). These mammals had their natural
possibly beneficial for human health (Oda et al. 1998; habitats largely wiped out due to deforestation. However,
Thorburn 2015; Wang and Brand-Miller 2003). Other bird they have adapted the pads on their hands, feet and rump to
species such as the bald-headed bulbul Pycnonotus hualon enable them to move on the sharp edges of the limestone,
(Woxvold et al. 2009), and the limestone leaf-warbler making these karst-dependent primates more specialized to
Phylloscopus calciatilis (Alström et al. 2010) have been living in this unique ecosystem (FFI 2001).
discovered only recently in Laos and Vietnam.

Figure 5. Photograph of Platymantis bayani in Taft (photograph by C. Siler) and a map (right) showing its known occurrence in eastern
Samar Island, Philippines (black dot). The inset shows the location of the species in Samar Island (colored black) within the Philippines.
The three provinces of Samar Island indicated by dashed lines (Siler 2009)
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1605

Invertebrates such as snails reach the peak of diversity or heterogeneity of the limestone landscapes poses a threat
and abundance in karst ecosystems especially because to many animal communities because they are deprived of
limestone which is made up of calcium carbonate is an habitats used for roosting and foraging-such as bats and
important component of their shells. The limestone birds. Hence, it is of high priority to understand how the
outcrops of Sabah, Malaysian Borneo hosts 74 species of environmental variables and landscapes in forest over
land snails (Prosobrasnchia and Pulmonata), and about 80 limestone are related to animal activities in order to
percent of the country’s total land snail fauna is found in effectively support efforts for their protection and
karst ecosystems (Schilthuizen 2000; Schilthuizen et al. conservation (Clements et al. 2008; Martin and Blackburn
2005). On another investigation by Haase and Schilthuizen 2010; Dias-Silva et al. 2018). This makes conservation
(2007), new limestone species of Georissa (Gastropoda: research essential in gathering important biological data
Neritopsina: Hydrocenidae) were collected from a karstic that policy makers should take into consideration to
limestone outcrop in Batu Sanaron, also found in Sabah, effectively put up laws that would benefit not only the
Malaysian Borneo. Asian karst ecosystem harbor about economy but concurrently being able to utilize natural
2000 species of snails which can be found only in the resources at a sustainable level while conserving its
region, of which, a single undisturbed karst hill may biodiversity.
contain about 60 to 100 different species (FFI 2001).
In the Philippines, there are only a few published
studies on the existing biological resources of limestone POTENTIALS OF FLORA AND FAUNA
ecosystems. A survey of Mt. Irid on the Southern Sierra BIODIVERSITY
Madre of Luzon Island recorded 8 species of non-volant
small mammals and 16 species of bats, including a new Research potential
island record for the lesser tube-nosed bat, Murina suilla Forests over limestone are largely understudied and the
(Balete et al. 2013). The island has also been the site of potential of discovering new flora and fauna species are
discovery for some karst-obligate frogs such as the data high. The effect of the unique morphology and features of
deficient Platymantis quezoni from the Quezon Protected limestone landscapes such as its caves, sinkholes, and
Landscape (Brown et al. 2015) and the near-threatened towers contribute to its low accessibility for research, but it
Platymantis biak from Biak Na Bato National Park (Siler has forced the flora and fauna species residing in the area
et al. 2010). Outside of Luzon Island, other karst-obligate to adapt, resulting to a unique and distinct organism
frogs include the endangered Platymantis spelaeus from composition. If the difficulty in research can be overcome,
Negros Island (Brown and Alcala 1982), the endangered the possibility of discovering new endemic species in the
Platymantis paengi from Panay Island (Siler et al. 2007), area is very high.
and the critically-endangered Platymantis insilatus from The presence or absence of flora and fauna species in
South Gigantes Island (Brown and Alcala 1970). In the forest over limestone could be indicators of the potential
Romblon Island Group, karst-dwelling lizards such as for further classifying limestone forests. Unlike dipterocarp
Gekko coi and Gekko romblon are known to occur (Siler et forests which usually have dominant flora species
al. 2012). In Samar Island Natural Park (SINP), the post- throughout the area, forests over limestone have varied
biological assessment of faunal resources by Patindol species composition (Ranlund 2011). Given the varied
(2016) recorded 182 species of terrestrial vertebrates, of nature of species composition, Ranlund (2011) suggested
which, 121 species were birds, 20 were mammals, 18 that in order to get an accurate description of limestone
amphibians and 23 reptiles with overall endemism of 40%. forests, it is not enough to select a single area and expect
This implies a great opportunity to discover new island the results to define the whole limestone landscape. To tap
records and possibly new species or taxa of wildlife in the great potential for discovery of new species, methods
forests over limestone. A good example is the karst forest involving spatial variation within limestone forests are
frog Platymantis bayani (Figure 5) described by Siler et al. recommended.
(2009) in the Taft Forest Reserve in eastern Samar Island,
the Philippines from an elevation of 140 m. Economic potential
Important information on the distribution and ecology In Southeast Asia, the natural occurrence of cave
of a wide array of wildlife can be discovered from future swiftlets provides a major industry in harvesting of nests
researches in the limestone ecosystem. A table showing the and at present appears to be ecologically sustainable.
compiled number of faunal species found in forests over However, any such industry should be monitored to ensure
limestone of Southeast Asia from different studies is shown that over-harvesting does not occur (Watson et al. 1997).
in Table 2. Bats are also economically important as they help in the
Economic development caused the extirpation of many pollination of numerous tree crops and consume insects
limestone-confined species including small and little- that damage agricultural crops. Biodiversity plays an
known invertebrates and only a few are included in the important role in maintaining existing karst landscapes and
IUCN Red List of Threatened Species (FFI 2001). gives foundation in the process of degraded karst
Increasing anthropogenic activities lead to conversion and ecosystem recovery (Jiang et al. 2014) which is important
alteration of natural landscapes that create harsh for future resource management plans.
environment for native species. The decreasing complexity
1606 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

Table 2. Major animal groups and the number of species found in different forests over limestone of Southeast Asia based from recent
faunal surveys

Major animal No. of


Location Notes Reference
group species
Birds 121 Samar Island Natural Park, Species might be included but are not Patindol (2016)
Philippines limited to forests over limestone.
1 Argao Watershed Reserve, Cebu, Black Shama Copsychus cebuensis Malaki et al. (2018)
Philippines Steere, 1890; Cebu endemic
129 Bau karsts, Sarawak, Malaysia 40 families Yong et al. (2004);
Clements (2006)
1 Limestone karst forests of the Nonggang Babbler Stachyris Jiang et al. (2019)
Sino-Vietnam border nonggangensis; rare and newly
discovered species that is restricted to
limestone karst forest on the Sino-
Vietnamese border
Reptiles 23 Samar Island Natural Park, Species might be included but are not Patindol (2016)
Philippines limited to forests over limestone.
11 Caves and karsts of Thailand Bent-toed geckos (genus Ellis and Pauwels (2012)
Cyrtodactylus); majority have a very
restricted geographical distribution.
15 Myanmar New species of Cyrtodactylus Grismer et al. (2018a,b)
(Squamata: Gekkonidae)
3 Malaysia New species of Cyrtodactylus Grismer et al. (2014a,c);
(Squamata: Gekkonidae) Grismer 2016
14 Malaysia New species of Cnemaspis Strauch Grismer et al. (2008a,b);
1887 (Squamata: Gekkonidae) Grismer (2009); Grismer
(2010);
Grismer (2013);
Grismer (2014b)
Amphibians 18 Samar Island Natural Park, Species might be included but are not Patindol (2016)
Philippines limited to forests over limestone.
1 Panay Island, Philippines Limestone-forest frog Siler et al. (2007)
1 Eastern Samar Island, Philippines Limestone-forest frog Siler et al. (2009)
1 Central Luzon Island, Philippines Limestone-forest frog Siler et al. (2010)
1 Khao Chang karst tower in Cave dwelling Ansonia Stoliczka Grismer (2017)
Phangnga Province, in southern (Anura: Bufonidae) species with
Thailand significant departure from lotic
lifestyle common to most other
species.
Mammals 20 Samar Island Natural Park, Species might be included but are not Patindol (2016)
Philippines limited to forests over limestone.
1 Cebu, Philippines Endangered Philippine tube-nosed Alburo (2017)
fruit bat Nyctimene rabori
1 Mt. Aruyan, Mindoro, Philippines Status of Tamaraw (Bubalus Matsubayashi et al.
mindorensis) (2010)
24 Mt. Irid, Southern Sierra Madre, 8 non-volant species and 16 species of Balete et al. (2013)
Luzon bats
9 Bicol Volcanic Belt, Southern Native species-1 shrew and 5 rodents; Balete et al. (2013)
Luzon, Philippines exotic species-1 shrew and 2 rodents.
1 Limestone hills of Merapoh, Petaurista petaurista (Pallas, 1766) Miard et al. (2020)
Malaysia (Mammalia: Rodentia: Sciuridae)
28 Mulu karsts, Sarawak, Malaysia Bat species Clements (2006)
36 Vietnamese limestone karst 5 families of bats Furey (2010)
6 Vietnam and Laos Limestone langurs genus Liu et al. (2019);
Trachypithecus: 1 found only in Laos Steinmetz et al. (2011)
(Steinmetz et al. 2011), 1 in
Southwestern China to northeastern
Vietnam, 1 in both Laos and Vietnam,
3 only in Vietnam.
12 Thailand Murid species Latinne et al. (2013)
Invertebrates 1 Barangay Bagong Silang, Basey First record of the genus Ermilov and Corpuz-
municipality, Western Samar Sacculogalumna (Acari: Oribatida: Raros (2017)
province, Samar Island, Galumnidae) from the Philippines.
Philippines
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1607

44 Borneo All recorded only from karsts. Vermeulen (1994);


Schilthuizen (2004);
Clements (2006)
122 Perak, Peninsular Malaysia 34 species unique to one of the Foon (2017)
surveyed hills; 30 species new to
science.
78 Peninsular Malaysia All species restricted to single isolated Davison (1991)
karsts
6 Sarang karst, Borneo All site endemics Vermeulen and Witten
50 Subis Karst, Malaysia No less than 50 species are endemic to (1999)
Subis Karst.
74 Sabah, Malaysian Borneo Pulmonate and Prosobranch land snails Schilthuizen (2005)
33 Sukolilo Karst, Java, Indonesia 13 families, 25 genera, 2 subspecies; 1 Nurinsiyah (2015).
new record to Java; 4 endemic species

Ecotourism also takes part in uplifting the limestone Pinarok et al. (2015) on SINP, all 62 species of plants (of
landscape’s economic potential. Aside from stunning which 6 are Philippine endemics) mostly represented by
sceneries and landscapes, tourists also visit to experience families Rubiaceae, Zingiberaceae, and Asteraceae have
the unique and wide array of flora and fauna, thereby medicinal uses. Aside from medicine, plants are also used
generating local employment. Biodiversity assessment can as raw materials for manufacturing food and other local
uncover new records and new species or taxa of flora and products that can be unique in that place only. While
fauna which will strengthen conservation efforts in such utilizing this potential is beneficial to communities, it is
areas. For example, species of ornamental plants such as equally important, or even more so, that conservation
Hoya (Apocynaceae) can be uncovered from the vastly efforts are done. Balancing the protection, resource
unexplored areas of Samar’s forests over limestone utilization, livelihood, and tourism in limestone landscapes
including Hoya cutis-porcelana which is endemic to Samar is essential for the socio-economic well-being of local
and Biliran Islands, Philippines (Aurigue et al. 2013). communities and sustainability of the area (Chechina et al.
Species of Philippine Hoyas described, published as new to 2018).
science, and collected from their natural habitats are
worthy of propagation for conservation and
commercialization purposes (Simonsson and Rodda 2009; CONSERVATION OF FOREST OVER LIMESTONE
Aurigue 2012; Aurigue et al. 2013; Kloppenburg et al.
2012; Kloppenburg et al. 2011; Kloppenburg et al. 2010a- Threats to limestone landscapes
d, 2011; Kloppenburg and Siar 2006a-c, 2008, 2009, 2010). Several factors contribute to creating drastic impacts on
Media in the form of photos, videos, and forests over limestone, affecting it in a negative way either
cinematography can also be a source of income while at the directly, indirectly, or both. Many of which are large-scale
same time promoting the value of protecting the events that endanger the very integrity or even survival of
environment to conserve the country’s unique biodiversity. the karst itself (Hamilton-Smith 2001). In Southeast Asian
The growing ecotourism industry generates a huge amount karsts, threats include limestone quarrying, land-use change
of money for economies around the world. In Malaysia, (Figure 6), deforestation, hunting, illegal logging
millions of dollars were invested for the majestic view of (Gillieson 2005; Lillo et al. 2019; Van Der Ploeg et al.
karst preserved as aesthetic backdrop for resort township 2011), and habitat degradation by process such as grazing
that provided opportunities for local residents to generate of domesticated animals and wood collection for fuel
income (Clements et al. 2006). In the Philippines, the (Clements et al. 2006; Woxvold et al. 2009).
stunning Taraw Cliff, an enormous limestone karst Environmental Impact Assessments (EIA) should be done
overlooking the town of El Nido, Palawan, serves as one of to know the possible extent of ecosystem biodiversity loss
the most popular ecotourism destinations in the country from proposed projects that would alter natural habitats and
which attracts a lot of local and foreign tourists. However, what can be done for it to be ecologically feasible (Bullecer
tourism should still be carefully regulated as a study in the 2014). The steady increase in human population also
karst area of Bantimurung Bulusaraung National Park, endangers the fragile ecosystem because of the increase in
Indonesia, which showed that there is a decrease presence consumption of natural resources. All of these factors pose
of birds in crowded tourist areas (Putri et al. 2019). a threat to the natural landscape and biodiversity of forest
Forests over limestone offer utilization of biological over limestone. Caves are given the most attention when it
resources and the chance of discovering new medicinal comes to protection of karst features, making other
plant species. The extensive range of flora that can be limestone landscapes of less consideration when it comes
found on forest over limestone offers a large window of to sustainable management and protection of the karst areas
opportunity which can unveil plants of significant health as a whole land unit (Watson et al. 1997). All other human
and economic importance such as plant-based drugs and uses of karst resources should be planned and monitored in
medicine. For instance, in an ethnobotanical survey by order to minimize undesirable impacts and to provide
information for future decision-making.
1608 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

Basey, Suribao and Catubig for its faunal resources. The


second study, on the other hand, assessed characteristics of
the floral diversity status in SINP and provided
recommendations on how such sources can be better
managed and protected against destruction (Quimio 2016).
Thus, the program “Assessment and Conservation of Forest
over Limestone Ecosystem Biodiversity in Selected
Municipalities of Samar Island, Philippines (CONserve-
KAIGANGAN)” was started in January of year 2019. It is
a 3-year research program funded by the Department of
Science and Technology-Philippine Council for
Agriculture, Aquatic and Natural Resources Research and
Development (DOST-PCAARRD) that aims to assess and
conserve the plant, animal and microbial diversity in
forests over limestone, "kaigangan" in Samar local dialect,
towards its sustainable management in Samar Island,
Figure 6. Land conversion into an agricultural area in SINP which Philippines.
poses a threat to karst landscapes. Photograph by P.J. Tolentino
Specific government initiatives for the protection of
karst biodiversity are attainable such as declaration of
National Parks (NPs) and other Protected Areas (PAs), and
public education. Declaration of NPs and other PAs have
Quarrying is one of the most destructive threats that
the best potential of protecting the total environment
need immediate action. In Peninsular Malaysia, at least 18
systems such as a karst ecosystem (Hamilton-Smith 2001),
karst-dependent plant species have been reported to have
but aside from declaring it as parks and inviting people to
gone extinct due to quarrying (Kiew 1991). Limestone is
visit, it must be noted that providing adequate and
so valuable for creating cement, that governments from
appropriate support for the management and protection of
developing countries are willing to overlook sustainable
such areas should not be neglected (Vimal et al. 2018).
limestone quarrying policies just to improve their economy
Increase in expenditure by the government on the
(Bambang and Utomo 2003; Galindon et al. 2018; Liew et
protection and research of these resources is essential for
al. 2016). Land-use planning that considers the welfare of
the acquisition of knowledge and professional education
poorer communities must be highlighted to address this.
for the community and land managers. Local community
Another problem at present is that there is lack of
participation is also important for management to ensure
information about how limestone forests fully support such
the integrity of NPs and PAs (Andrade and Rhodes 2012).
biodiversity. Thus, thorough research is required to
In the South China Karst landscapes, for example, a
implement conservation strategies that will influence the
monitoring index (Table 3) for measuring state of
use of such resources at a sustainable level. Understanding
conservation has been established. The monitoring index is
the present-day situation through research will help
made for the nominated karst areas of South China but it
develop rational strategies with particular reference to karst
can also be applicable to other karst areas especially in
such as appropriate land management, sustainable land use
other Southeast Asian countries where tropical karst areas
planning, and expansion and maintenance of protected
are found.
areas (Day 2010). The high endemicity and fragile nature
About 29% of the total karst landscape in the
of flora and fauna in forest over limestone are important in
Philippines is protected. There is no existing legislation
determining proper conservation techniques. This high
that directly addressed its protection and conservation in
endemicity and high chance of discovering new species is
the country; however, there is other legislation that
an opportunity for researchers to explore limestone
indirectly protects karst landscapes (Table 4). Tourism is
landscapes.
one of the main reasons for karst conservation while other
karst landscapes are indirectly protected only because
Conservation of limestone landscapes
portions of it are covered within a larger protected area
In relation with biodiversity research, recent studies,
such as nature reserves, natural parks, wildlife sanctuary, or
related to but not specifically, about the forest over
protected seascapes (Restificar et al. 2006). Holistic
limestone of the Philippines were done in Samar Island
research of the limestone areas is critical to be able to
Natural Park by Patindol (2016) and Quimio (2016)
establish scientific and knowledge-based initiatives and
entitled Post Biological Assessment of Faunal Resources in
laws that will conserve the Philippine forests over
the Samar Island Natural Park (SINP), and Floral
limestone biodiversity while at the same time being able to
Composition and Timber Stock of Forest in the Samar
utilize it at a sustainable level.
Island Natural Park, respectively. The first study surveyed
5 priority watersheds of SINP namely Taft, Can-avid,
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1609

Table 3. Monitoring index for conservation of South China Karst landscapes implemented by the government (Jiang et al. 2014)

Parameter Resolution
Karst monitoring processes Solution rate, dynamic hydrology and elements of surface and underground water
Ecological processes and biodiversity Monitoring on vegetations, observation of animals, changes of animal species, vegetation
monitoring meteorological phenomena, quality of species and cave animals species, monitoring on
exotic species
Environmental monitoring Observation of atmosphere, waters, noise and environmental health
Land using monitoring Cropland, construction, water, mining, logging, afforestation and transportation facilities
Visitors administering monitoring Number of visitors, tourism items, scenic spot, quality and quantity of tourism facilities
Natural disasters monitoring Meteorologic disasters, fire, drought and flood, mud-rock flow, ground sinking,
earthquakes, etc.

Table 4. Legislations that indirectly protect limestone landscapes in the Philippines (Restificar et al. 2006)

Legislation Objective
Republic Act 9147 or the “Wildlife Resources Conservation and Aims to conserve the country’s wildlife resources and their
Protection Act” habitats, and can be used to protect wildlife resources in specific
karst areas
Republic Act 7942 or the “Mining Act” Contains provisions relating to areas closed to mining operations.
These include all areas under NIPAS, which includes several karst
areas
DENR-DOT Memorandum Circular 98-02 (Guidelines for Provide guidelines for the management of caves used for
Ecotourism Development in the Philippines) and Executive Order ecotourism activities
No. 11 (Establishing the Guidelines for Ecotourism Development
in the Philippines)
Republic Act 4846 or the “Cultural Properties Preservation and May be invoked to protect cave resources of cultural significance
Protection Act”

The importance of public education can never be indirectly protected mainly because it is included in wider
neglected. The decisions of the public upon the areas specified for protection. Unfortunately, there are no
legitimization of government actions is important for the legislation that directly address the conservation of forests
development of effective forest over limestone protection. over limestone. Although the whole karst landscapes are
It is necessary to educate park managers, tourists, and the not assigned as protected areas, land managers should
community with gathered scientific knowledge so they will continually try to establish well-planned and knowledge-
have better understanding and make appropriate decisions. based conservation procedures for its protection. There is
Public education can also be done through interpretation at an opportunity and a need to study limestone forests
parks, journalism, electronic media and popular books for further. The combination of unique species, valuable
all ages (Hamilton-Smith 2001). Community forestry, resources in the form of forest products, limestone and
when applicable, has proven to be an effective and water, and its fragility makes its conservation of utmost
sustainable means of limestone forest conservation. importance. The first step is to increase research efforts in
Community Forestry in Thailand is legally recognized as forests over limestone. This is important since the current
the participation of a community with forestry officers in baseline information on biodiversity is not sufficient in
forest management activities under laws and regulations most areas to create proper management strategies in forest
(Laosuksri and Qi 2014). The community maintains their over limestone. Conducting regular monitoring and
culture and other traditions, and they are free to utilize the evaluation activities for biodiversity on forest over
forest to sustain their needs while simultaneously focusing limestone areas is crucial to know the integration of
on conservation and development. The cooperation of the species, ecosystems, and the landscape itself. Aside from
community on reforestation creates a sense of involvement resource protection knowledge, there is also a demand for
in forest conservation among the villagers. the unity of local communities and the government in order
to effectively conserve the environment. If people are
equipped with knowledge that these further studies will
CONCLUDING REMARKS provide, communities will be able to know more of what
forests over limestone can offer, and thus implement proper
Forests over limestone are geomorphologically unique forest management strategies for its protection and
but fragile landscapes. They contain a high degree and conservation while at the same time being able to utilize its
extensive range of biodiversity and remains mostly biological resources at a sustainable level.
unexplored. In the Philippines, many karst areas are
1610 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

ACKNOWLEDGEMENTS http://www.bmb.gov.ph/bmb/CAWED/Proposed_Policy/CMPCSAP_
2019-2028.pdf?cv=1.
Brown RM, De Layola LA, Ii AL, Diesmos MLL, Diesmos AC. 2015. A
The authors would like to thank the Institute of new species of limestone karst inhabiting forest frog, genus
Biological Sciences of the University of the Philippines, Platymantis (Amphibia: Anura: Ceratobatrachidae: Subgenus
Los Baños, Laguna, and DOST-PCAARRD for its funded Lupacolus) from southern Luzon Island, Philippines. Zootaxa 4048
(2): 191-210. DOI: 10.11646/zootaxa.4048.2.3
program: Assessment and conservation of forest over Brown WC, Alcala AC. 1982. A new cave Platymantis (Amphibia:
limestone ecosystem biodiversity in selected municipalities Ranidae) from the Philippine Islands. Proc Biol Soc Washington 95
of Samar, Philippines (CONserve-KAIGANGAN) Project (2): 386.
1: Assessment of Biodiversity in forest over limestone Brown WC, Alcala AC. 1970. A new species of the genus Platymantis
(Ranidae) with a list of amphibians known from South Gigante
ecosystem. We would also like to thank the DOST Science Island, Philippines. Occas Pap California Acad Sci 84: 1-7.
Education Institute (SEI) for allowing the fifth author to Bullecer RC, Reyes TD Jr, Labonite MA, Jose RP, Lomosbog NT,
take part in this research program through the Career Labonite EKA, Ancog AB, Travero JT, Bautista BA Jr. 2014. Mega
Incentive Program (CIP). construction in Panglao Island, Philippines: The magnitude of the
possible biodiversity losses. Intl J Environ Rural Dev 5 (2): 137-142.
Cadiz GO, Buot IE. 2010. An enumeration of the vascular plants of Mount
Tabunan, Cebu Island, Philippines. Thailand Nat Hist Mus J 4 (2):
REFERENCES 71-77.
Cadiz GO, Buot IE. 2011. Physico-chemical factors affecting the vascular
plant diversity of lowland forest in Mount Tabunan, Cebu Island,
Adam JH, Mamat Z. 2005. Floristic composition and structural
Philippines. Asia Life Sci 6: 1-12.
comparison of limestone forests at three different elevations in Bau,
Calumpong HP. 2014. The flora of the limestone forest of Baladingan,
Kuching, Sarawak, Malaysia.
Ticao Island, Philippines. EM Intl. Spec Issue-2014: 11-23.
Adorador J, Fernando E. 2019. Orania zheae (Oranieae, Arecoideae,
Chechina M, Neveux Y, Parkins JR, Andreas H. 2018. Balancing
Arecaceae), a new species from the Philippines, with notes on another
conservation and livelihoods: A study of forest-dependent
slender-stemmed species. Phytotaxa 391: 69. DOI:
communities in the Philippines. Conserv Soc 16 (4): 420-30. DOI:
10.11646/phytotaxa.391.1.5.
10.4103/cs.cs_16_182.
Adorador J, Fernando E. 2017. Palms of Samar Island, Philippines. Palms
Chen WH, Zhang YM, Li ZY, Nguyen QH, Nguyen TH, Shui Y. 2018.
61 (4).
Hemiboea crystallina, a new species of Gesneriaceae from karst
Adorador J, Meneses Z, Fernando E. 2020. Pinanga gruezoi (Araceae), a
regions of China and Vietnam. Phytotaxa 336 (95). DOI:
new slender clustering palm from the Philippines with notes on an
10.11646/phytotaxa.336.1.8.
amended description of P. samarana. Phytotaxa 429 (2). DOI:
Chin SC. 1977. The limestone hill flora of Malaya: Part 1. Gard Bull Sing
10.11646/phytotaxa.429.2.3.
30: 165-220.
Alburo H. 2018. Abundance and distribution of Philippine Tube-nosed
Clements R, Ng PKL, Lu XX, Ambu S, Schilthuizen M, Bradshaw CJA.
Fruit Bat in Cebu, Philippines. J Soc Technol 7: 19-29.
2008. Using biogeographical patterns of endemic land snails to
Alström P, Davidson P, Duckworth JW, Eames JC, Le TT, Nguyen C,
improve conservation planning for limestone karsts. Biol Conserv 141
Timmins R. 2010. Description of a new species of Phylloscopus
(11): 2751-2764. ISSN 0006-3207.
warbler from Vietnam and Laos. Ibis 152 (1): 145-168. DOI:
Clements R, Sodhi NS, Schilthuizen M, Ng PKL. 2006. Limestone karsts
10.1111/j.1474-919X.2009.00990.x
of Southeast Asia: Imperiled arks of biodiversity. BioScience 56 (9):
Andrade G, Rhodes J. 2012. Protected areas and local communities: An
733. DOI: 10.1641/0006-3568 (2006)56[733:lkosai]2.0.co;2.
inevitable partnership toward successful conservation strategies?.
Connette GM, Oswald P, Thura MK, Connette KJL, Grindley ME, Songer
Ecol Soc 17. DOI: 10.5751/ES-05216-170414.
M, Mulcahy DG. 2017. Rapid forest clearing in a Myanmar proposed
Asanok L, Marod D. 2016. Environmental factors influencing tree species
national park threatens two newly discovered species of geckos
regeneration in different forest stands growing on a limestone hill in
(Gekkonidae: Cyrtodactylus). PLoS ONE 12 (4). DOI:
Phrae Province, Northern Thailand. J For Environ Sci 32 (3): 237-
10.1371/journal.pone.0174432.
252. DOI: 10.7747/jfes.2016.32.3.237.
Co LL, Lagunzad DA, Pasion KAC, Consunji HT, Bartolome NA, Yap
Aurigue F. 2012. Updates on Philippine Hoyas. Philippine Hortic Primer
SL, Molina JE, Tongco MDC, Ferreras UF, LaFrankie JV, Davies SJ,
Dir 3: 28-33.
Ashton PS. 2006. Forest trees of Palanan, Philippines: A Study in
Aurigue F, Sahagun J, Suarez W. 2013. Hoya cutis-porcelana
Population Ecology. Center for Tropical Forest Science. Center for
(Apocynaceae): A new species from Samar and Biliran islands,
Integrative and Development Studies, University of the Philippines-
Philippines. J Nat Stud 12 (1): 12-17.
Diliman, Quezon City, Philippines.
Balete DS, Heaney LR, Alviola P, Rickart EA. 2013. Diversity and
Dang NX, Nghia NX, The PV. 2019. The Tonkin snub-nosed monkey
distribution of small mammals in the Bicol Volcanic Belt of Southern
Rhinopithecus avunculus population in the Quan Ba forest, north-east
Luzon Island, Philippines. Natl Mus Philippines J Nat Hist 1: 61-86.
Vietnam: an identification of priority habitat for conservation. Acad J
Balete DS, Heaney LR, Rickart EA. 2013. The mammals of Mt. Irid,
Biol 41 (3): 47-54 DOI: 10.15625/2615-0923/v41n3.13799.
Southern Sierra Madre, Luzon Island, Philippines. Natl Mus
Davison GWH. 1991. Terrestrial molluscs of Peninsular Malaysia. Pages
Philippines J Nat Hist 15-21.
101-104. In: Kiew R, (eds) The State of Nature Conservation in
Bambang M, Utomo GW. 2003. Limestone quarries ruin Gunungkidul’s
Malaysia. Kuala Lumpur (Malaysia): Malayan Nature Society.
beauty. Jarkata Post, 17. [Indonesian]
Day M, Urich P. 2000. An assessment of protected karst landscapes in
Barcelona JF, Dolotina NE, Madroñero GS, Granert WG, Sopot DD.
Southeast Asia. Cave Karst Sci 27 (2): 61-70.
2006. The ferns and fern allies of the karst forests of Bohol Island,
Day M. 2010. Human interaction with Caribbean Karst Landscapes: Past,
Philippines. Am Fern J 96 (1): 1-20. DOI: 10.1640/0002-8444
present and future. Acta Carsol 39 (1): 137-146. DOI:
(2006)96[1:tfafao]2.0.co;2.
10.3986/ac.v39i1.119.
Binh LV, Nguyen VT, Köpp R, Hai VD, Mitloehner R. 2015. Responses
Dehling JM. 2011. A new karst-dwelling species of Kalophrynus (Anura:
of native tree species to soil water stress in a tropical forest on
Microhylidae) from Gunung Mulu National Park, Borneo, Malaysia.
limestone, Vietnam. Open J For 05: 711-722. DOI:
Zootaxa 2737: 49-60.
10.4236/ojf.2015.57063.
Dias-Silva L, Duarte GT, Alves R, Pereira MJR, Paglia A. 2018. Feeding
BirdLife/FFI/IUCN/WWF. 2014. Joint briefing paper on extraction and
and social activity of insectivorous bats in a complex landscape: The
biodiversity in limestone areas. Cambridge, UK, 1-4. Retrieved from
importance of gallery forests and karst areas. Mammal Biol 88: 52-63.
https://www.birdlife.org/sites/default/files/Extraction-and-
DOI: 10.1016/j.mambio.2017.11.005.
Biodiversity-in-Limestone-Areas.pdf.
Ellis M, Pauwels OSG. 2012. The bent-toed geckos (Cyrtodactylus) of the
BMB-DENR. 2019. Protection and Conservation Strategy and Action
caves and karst of Thailand. Cave Karst Sci 39 (1): 16-22.
Plan. Retrieved from
Ermilov SG, Corpuz-Raros L. 2017. First record of the genus
Sacculogalumna (Acari: Oribatida: Galumnidae) from the
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1611

Philippines, with description of a new species. Trop Zool 30 (3): 125- and unprecedented microendemism. Zool J Linn Soc 182 (4): 862-
134. DOI: 10.1080/03946975.2017.1345512. 959. DOI: 10.1093/zoolinnean/zlx057.
Fernando ES, Suh MN, Lee J, Lee DK. 2008. Forest formation of the Haase M, Schilthuizen M. 2007. A new Georissa (Gastropoda:
Philippines. ASEAN-Korea Environmental Cooperation Unit Neritopsina: Hydrocenidae) from a limestone cave in Malaysian
(AKECU). Securing the future for Asia’s stunning karst ecosystems. Borneo. J Molluscan Stud 73 (3): 215-221. DOI:
Flora Fauna Int 1-8. 10.1093/mollus/eym020.
Foon JK, Clements GR, Liew T-S. 2017. Diversity and biogeography of Hamilton-Smith E. 2001. Current initiatives in the protection of karst
land snails (Mollusca, Gastropoda) in the limestone hills of Perak, biodiversity. Nat Croatica 10 (3): 229-242.
Peninsular Malaysia. ZooKeys 682: 1-94. DOI: Hetterscheid W, Wistuba A, Amoroso V, Medecilo M, Claudel C. 2012.
10.3897/zookeys.682.12999. Amorphophallus natolii (Araceae), a new species from limestone on
Furey NM, Mackie IJ, Racey PA. 2010. Bat diversity in Vietnamese Palawan, Philippines. Bot Stud 53: 415-420.
limestone karst areas and the implications of forest degradation. Jenkins PD, Kilpatrick WC, Robinson M, Timmins RJ. 2005.
Biodivers Conserv 19 (7): 1821-1838. DOI: 10.1007/s10531-010- Morphological and molecular investigations of a new family, genus
9806-0. and species of rodent (Mammalia: Rodentia: Hystricognatha) from
Galindon JM, Pasion B, Tongco MD, Fidelino J, Duya MR, Ong P. 2018. Lao PDR. Syst Biodivers 2 (4): 419-454. DOI:
Plant diversity patterns in remnant forests and exotic tree species- 10.1017/S1477200004001549.
based reforestation in active limestones quarries in the Luzon and Jiang D, Goodale E, Yang G, Yu L, Aiwu J, Luo X. 2019. Modeling the
Mindanao biogeographic sub-regions in the Philippines. Ecol Res 33 distribution of Nonggang Babbler Stachyris nonggangensis, a
(1): 63-72. DOI: 10.1007/s11284-017-1533-5. threatened bird of limestone karst forests of the Sino-Vietnam border,
Gillieson D. 2005. Karst in Southeast Asia. Phys Geogr Southeast Asia and implications for its conservation. Bird Conserv Int 1-12. DOI:
157-176. 10.1017/S0959270919000236.
Grismer LL, Belabut DM, Quah ESH, Onn CK, Wood PL, Hasim R. Jiang Z, Lian Y, Qin X. 2014. Rocky desertification in Southwest China:
2014a. A new species of karst forest-adapted Bent-toed Gecko (genus Impacts, causes, and restoration. Earth-Sci Rev 132: 1-12. DOI:
Cyrtodactylus Gray, 1827) belonging to the C. sworderi complex 10.1016/j.earscirev.2014.01.005.
from a threatened karst forest in Perak, Peninsular Malaysia. Zootaxa Kiew R. 2014. Checklist of vascular plants from Batu Caves, Selangor,
3755 (5): 434-446. DOI: 10.11646/zootaxa.3755.5.3. Malaysia. Check List 10 (6): 1420-1429. DOI: 10.15560/10.6.1420
Grismer LL, Grismer JL, Wood PLJ, Onn CK. 2008a. The distribution, Kiew R. 2016. Impatiens (Balsaminaceae) species from karst limestone in
taxonomy, and redescription of the geckos Cnemaspis affinis Kelantan, Malaysia, including three new species. Gard Bull Singap
(Stoliczka 1887) and C. flavolineata (Nicholls 1949) with 68: 225. DOI: 10.3850/S2382581216000181.
descriptions of a new montane species and two new lowland, karst- Kiew R. 1991. The limestone flora. In: Kiew R (eds). The State of Nature
dwelling species from Peninsular Malaysia. Zootaxa 1931: 1-24. Conservation in Malaysia. Malayan Nat Soc, Kuala Lumpur 42-50.
Grismer LL, Onn CK. 2009. A new species of karst dwelling Cnemaspis Kingston T. 2008. Research priorities for bat conservation in Southeast
Strauch 1887 (Squamata: Gekkonidae) from Sarawak, Borneo. Asia: A consensus approach. Biodivers Conserv 19 (2): 471-484.
Zootaxa 2246: 21-31. DOI: 10.11646/zootaxa.2246.1.2. DOI: 10.1007/s10531-008-9458-5.
Grismer LL, Onn CK. 2010. Another new Rock Gecko (genus Cnemaspis Kingston T, Francis CM, Akbar Z, Kunz TH. 2003. Species richness in an
Strauch 1887) from Pulau Langkawi, Kedah, Peninsular Malaysia. insectivorous bat assemblage from Malaysia. J Trop Ecol 19 (1): 67-
Zootaxa 2419: 51-62. DOI: 10.11646/zootaxa.2419.1.2. 79. DOI: 10.1017/S0266467403003080.
Grismer LL, Onn CK, Nasi N, Sumontha M. 2008b. A new species of Kloppenburg RD, Guevarra MLD, Carandang JM, Maranan FS. 2012.
karst dwelling gecko ( genus Cnemaspis Strauch 1887 ) from the New Species of Hoya R. Br. (Apocynaceae) from the Philippines. J
border region of Thailand and Peninsular Malaysia. Zootaxa 1875: Nat Stud 11 (1&2): 34-48.
51-68. DOI: 10.5281/zenodo.184071. Kloppenburg RD, Siar SV, Carandang JM, Hadsall AS. 2011. Hoya ilagii,
Grismer LL, Wood PL, Anuar S, Davis HR, Cobos AJ, Murdoch ML. another new species (Apocynaceae, Asclepiadoideae) from Luzon
2016. A new species of karst forest Bent-toed Gecko (genus Island, Philippines. Asia Life Sci 20 (2): 263-269.
Cyrtodactylus Gray) not yet threatened by foreign cement companies Kloppenburg RD, Siar SV, Ferreras UF. 2011. Hoya amrita Kloppenburg,
and a summary of Peninsular Malaysia’s endemic karst forest Siar & Ferreras sp. nova. Asclepios110: 27-29.
herpetofauna and the need for its conservation. Zootaxa 4061: 1-17. Kloppenburg RD, Siar SV, Ferreras, UF. 2010a. Hoya kanlaonensis
Grismer LL, Wood PL, Anuar S, Riyanto A, Ahmad N, Muin MA, Kloppenburg, Siar & Ferreras. Fraterna 23 (4): 24-27.
Pauwels OSA. 2014b. Systematics and natural history of Southeast Kloppenburg RD, Siar SV, Ferreras, UF. 2010b. Hoya ferrerasii
Asian Rock Geckos (genus Cnemaspis Strauch, 1887) with Kloppenburg & Siar sp. nova. Fraterna 23 (4): 21-23.
descriptions of eight new species from Malaysia, Thailand, and Kloppenburg RD, Siar SV, Ferreras, UF. 2010c. Hoya corazoniae
Indonesia. Zootaxa 3880: 1-147. Kloppenburg, Siar & Ferreras. Fraterna 23 (4): 15-19.
Grismer LL, Wood PL, Aowpho A, Cota M, Grismer MS, Murdoch ML, Kloppenburg RD, Siar SV, Ferreras, UF. 2010d. Hoya carmelae
Grismer JL. 2017. Out of Borneo, again and again: Biogeography of Kloppenburg, Siar & Ferreras. Fraterna 23 (4): 9-13.
the Stream Toad genus Ansonia Stoliczka (Anura: Bufonidae) and the Kloppenburg RD, Siar SV. 2010. New species of Hoya (Apocynaceae)
discovery of the first limestone cave-dwelling species. Biol J Linn from Brunei and the Philippines. Gard Bull Singap 61 (2): 87-94.
Soc 120 (2): 371-395. DOI: 10.1111/bij.12886. Kloppenburg RD, Siar SV. 2009. Additional four new species of Hoya
Grismer LL, Wood PL, Mohamed M, Chan KO, Heinz HM, Sumarli ASI, R.Br. (Apocynaceae) from the Philippines. Asia Life Sci 18 (1): 139-
Loredo AI. 2013. A new species of karst-adapted Cnemaspis Strauch, 154.
1887 (Squamata: Gekkonidae) from a threatened karst region in Kloppenburg RD, Siar SV. 2008. Three new species of Hoya R.Br.
Pahang, Peninsular Malaysia. Zootaxa 3746 (3): 463-472. DOI: (Apocynaceae) from the Philippines. Asia Life Sci 17 (1): 57-70.
10.11646/zootaxa.3746.3.5 Kloppenburg RD, Siar SV. 2006a. Hoya stoneiana Kloppenburg & Siar.
Grismer LL, Wood PL, Onn CK, Anuar S, Muin MA. 2014c. Cyrts in the Fraterna 19 (4): 19-23.
city: A new Bent-toed Gecko (genus Cyrtodactylus) is the only Kloppenburg RD, Siar SV. 2006b. Hoya linavergariae Kloppenburg &
endemic species of vertebrate from Batu Caves, Selangor, Peninsular Siar. Fraterna 19 (4): 11-18.
Malaysia. Zootaxa 3774 (4): 381-394. DOI: Kloppenburg RD, Siar SV. 2006c. Hoya lucyae Kloppenburg & Siar.
10.11646/zootaxa.3774.4.6. Fraterna 19 (4): 8-10.
Grismer LL, Wood PL, Thura MK, Quah ESH, Murdoch ML, Grismer Kumar P, Gale SW, Schuiteman A, Bouamanivong S, Fischer GA. 2016.
MS, Kyaw H. 2018a. Three more new species of Cyrtodactylus Identifying orchid hotspots for biodiversity conservation in Laos: the
(Squamata: Gekkonidae) from the Salween basin of eastern Myanmar limestone karst vegetation of Vang Vieng District, Vientiane
underscore the urgent need for the conservation of karst habitats. J Province. J Threatened Taxa 8 (12): 9397-9417. DOI:
Nat Hist 52 (19-20): 1243-1294. DOI: 10.11609/jott.2826.8.12.9397-9417
10.1080/00222933.2018.1449911. Laosuksri W, Qi G. 2014. Reforestation in limestone forest in Central
Grismer LL, Wood PL, Thura MK, Thaw ZIN, Quah ESH, Murdoch ML, Thailand : A case of Baan Lam Nam Kaew community forestry in
Lwin N. 2018b. Twelve new species of Cyrtodactylus Gray Lopburi Province. Civil Environ Res 6 (3): 59-66.
(Squamata: Gekkonidae) from isolated limestone habitats in east- Latinne A, Waengsothorn S, Herbreteau V, Michau J.R, Baillarguet CIDe.
central and southern Myanmar demonstrate high localized diversity 2011. Thai limestone karsts: An impending biodiversity crisis. Int
1612 B I OD I V E R S ITA S 21 (4): 1597-1613, April 2020

Conf Environ Support-Ing Food Energy Secure: Crisis Opportunity Vietnam). Trop Conserv Sci 326-341. DOI:
(March):176-187. 10.1177/194008291400700211.
Latinne A, Waengsothorn S, Rojanadilok P, Eiamampai K, Sribuarod K, Ngo VT. 2011. Cyrtodactylus martini, another new karst-dwelling
Michaux JR. 2013. Diversity and endemism of Murinae rodents in Cyrtodactylus Gray, 1827 (Squamata: Gekkonidae) from
Thai limestone karsts. Syst Biodivers 11 (3): 323-344. Northwestern Vietnam. Zootaxa 2834 (1): 33-46.
Liew T-S, Price L, Clements GR. 2016. Using Google Earth to Improve Nguyen NX, Nguyen DX, Ngo TX, Nguyen DD. 2015. New data on
the Management of Threatened Limestone Karst Ecosystems in recently described rodent species Paulina’s Limestone Rat
Peninsular Malaysia. Trop Conserv Sci 903-920. DOI: Saxatilomys paulinae Musser, Smith, Robinson & Lunde, 2005
10.1177/194008291600900219 (Mammalia: Rodentia). Biodivers Data J 3 (1). DOI:
Lillo EP, Fernando ES, Lillo MJR. 2019. Plant diversity and structure of 10.3897/BDJ.3.e4961
forest habitat types on Dinagat Island, Philippines. J Asia-Pacific Nguyen TQ, Van Pham A, Ziegler T, Ngo HT, Le MD. 2017. A new
Biodivers 12 (1): 83-105. DOI: 10.1016/j.japb.2018.07.003 species of Cyrtodactylus (Squamata: Gekkonidae) and the first record
Lillo EP, Malaki AB, Alcazar SMT, Rosales R, Redoblado BR, of C. otai from Son La Province, Vietnam. Zootaxa 4341 (1): 25-40.
Pantinople E, Buot IE Jr. 2020. Diversity and distribution of ferns in DOI: 10.11646/zootaxa.4341.1.2
forest over limestone in Cebu Island key biodiversity areas (KBAs), Nguyen TV, Mitloehner R, Bich NV, Do TV. 2015. Environmental factors
Philippines. Biodiversitas 21 (1): 413-421. DOI: affecting the abundance and presence of tree species in a tropical
10.13057/biodiv/d210148 lowland limestone and non-limestone forest in Ben En National Park,
Liu Z, Zhang L, Yan Z, Ren Z, Han F, Tan X, Xiang Z, Dong F, Yang Z, Vietnam. J For Environ Sci 31: 177-191. DOI:
Li G., Wang Z, Zhang J, Que T, Tang, Li, Y, Wang S, Wu J, Li L, 10.7747/JFES.2015.31.3.177.
Huang C, Li M. 2019. Genomic Mechanisms of Physiological and Nizam M, Rohani S, Wan Ahmad WJ. 2012. Floristic Variation of Tree
Morphological Adaptations of Limestone Langurs to Karst Habitats. Communities in Two Distinct Habitats within a Forest Park in
Mol Biol Evol. DOI: 10.1093/molbev/msz301. Pahang, Peninsular Malaysia. Sains Malaysiana 41: 1-10.
Luu VQ, Bonkowski M, Nguyen TQ, Le MD, Schneider N, Ngo HT, Norhazrina N, Syazwana N, Aisyah M, Aznani H, Maideen H, Nizam MS.
Ziegler T. 2016. Evolution in karst massifs: Cryptic diversity among 2019. Mosses of Gunung Senyum Recreational Forest, a tropical
bent-toed geckos along the Truong Son Range with descriptions of limestone forest in Pahang, Peninsular Malaysia. PhytoKeys 128: 57-
three new species and one new country record from Laos. Zootaxa 72. DOI: 10.3897/phytokeys.128.33860
4107 (2): 101-140. DOI: 10.11646/zootaxa.4107.2.1 Nurinsiyah A. 2015. Land Snail Fauna of the Sukolilo Karst in Java
Luu VQ, Nguyen TQ, Le MD, Bonkowski M, Ziegler T. 2016. A new (Indonesia). Am Conchol 43: 30-32.
species of karst-dwelling bent-Toed gecko (Squamata: Gekkonidae) Oda M, Ohta S, Suga T, Aoki T. 1998. Study on food components: The
from Khammouane Province, central Laos. Zootaxa 4079 (1): 87-102. structure of N-Linked Asialo Carbohydrate from the edible bird’s nest
DOI: 10.11646/zootaxa.4079.1.6 built by Collocalia fuciphaga. J Agric Food Chem 46 (8): 3047-3053.
Luu VQ, Nguyen TQ, Le MD, Bonkowski M, Ziegler T. 2017. A new Ordas JA, Pinarok N, Romeroso R, Alejandro GJ, Banag C. 2019. A
karst dwelling species of the Gekko japonicus group (Squamata: checklist of Rubiaceae species from Eastern Samar, Visayas,
Gekkonidae) from central Laos. Zootaxa 4263 (1): 179-193. Philippines. Check List 15: 295-312. DOI: 10.15560/15.2.295.
Malaki ABB, Cruz RVO, Bantayan NC, Racelis DA, Buot IE Jr., Florece Panitvong N, Lauhachinda V, Saithong S, Temchai T. 2012. Ecology of
LM. 2018. Factors affecting the spatial distribution of Black Shama Cyrtodactylus sumonthai Bauer, Pauwels, & Chanhome, 2002
Copsychus cebuensis Steere, 1890 in Argao Watershed Reserve. (Reptilia: Squamata: Gekkonidae): A karst dwelling bent-toed gecko
Philippine J Sci147 (1): 175-189. from south-eastern Thailand. Raffles Bull Zool 60 (2): 569-582.
Marcone MF. 2005. Characterization of the edible bird’s nest the “Caviar Patindol T. 2016. Post biological assessment of faunal resources in the
of the East.” Food Res Int 38 (10): 1125-1134. DOI: Samar Island Natural Park. Ann Trop Res 73: 52-73. DOI:
10.1016/j.foodres.2005.02.008 10.32945/atr3824.2016
Martin TE, Blackburn GA. 2010. Impacts of tropical forest disturbance Pauwels OSG, Sumontha M. 2014. Cyrtodactylus samroiyot, a new
upon avifauna on a small island with high endemism implications for limestone-dwelling Bent-toed Gecko (Squamata: Gekkonidae) from
conservation. Conserv Soc 8 (2): 127-139. DOI: 10.4103/0972- Prachuap Khiri Khan Province, peninsular Thailand. Zootaxa 3755
4923.68914. (6): 573-583. DOI: 10.11646/zootaxa.3755.6.4
Matsubayashi H, Boyles RM, Salac RL, Del Barrio A, Cruz LC, Garcia Pelser PB, Barcelona JF, Nickrent DL. 2011 onwards. Co’s Digital Flora
RA, Ishihara S, Kanai Y. 2010. Present status of Tamaraw (Bubalus of the Philippines. Available from: http://www. philippineplants.org
mindorensis) in Mt. Aruyan, Mindoro, Philippines. Tropics 18 (4): (accessed 7 May 2016)
167-170. Pelser PB, Nickrent DL, Reintar A, Barcelona JF. 2016. Lepeostegeres
Meneses ZD, Cootes JE. 2019. Pseuderia samarana (Orchidaceae), a new cebuensis (Loranthaceae), a new mistletoe species from Cebu,
species and genus record from the Philippines. Taiwania 64 (4): 353- Philippines. Phytotaxa 266: 48. DOI: 10.11646/phytotaxa.266.1.8.
356. Peng CI, Lin CW, Yang HA, Kono Y, Nguyen H. 2015. Six new species
Meneses ZD, Malabrigo PL Jr., Buot IE Jr., Tinio CE. 2018. New of Begonia (Begoniaceae) from limestone areas in Northern Vietnam.
distribution records of Orchids (Orchidaceae) in Samar Island, Bot Stud 56. DOI: 10.1186/s40529-015-0089-3.
Philippines. J Nat Stud 17 (2): 1-9. Peng CI, Rubite RR, Lin CW, Hughes M, Kono Y, Chung KF. 2017.
Miard P, Arifuddin MN, Mukri I, Sapno SS, Yazid H, Ruppert N, Three new species of Begonia sect. Baryandra from Panay Island,
Kumaran JV. 2020. Sighting of Petaurista petaurista (Pallas, 1766) Philippines. Bot Stud 58 (1): 28. DOI: 10.1186/s40529-017-0182-x
(Mammalia: Rodentia: Sciuridae) on limestone hills in Merapoh, Peque D, Hölscher D. 2014. The abundance of rare tree species in remnant
Malaysia. J Threatened Taxa 12 (3): 15355-15358. DOI: forests across the Visayas, Philippines. Biodivers Conserv 23. DOI:
10.11609/jott.5419.12.3.15355-15358. 10.1007/s10531-014-0714-6.
Mohamed H, Tan B. 1988. A Checklist of Mosses of Peninsular Malaya Pérez-García E, Sevilha A, Meave J, Scariot A. 2009. Floristic
and Singapore. The Bryologist 91 (1): 24-44. doi:10.2307/3242736 differentiation in limestone outcrops of Southern Mexico and Central
Mohamed H, Yong KT, Damanhuri A, Latiff QA. 2005. Moss diversity of Brazil: A beta diversity approach. Boletín de La Sociedad Botánica de
Langkawi Islands, Peninsular Malaysia. Malayan Nat J 57: 243-254. México 84: 45-58.
Musser GG, Smith AL, Robinson MF, Lunde DP. 2005. Description of a Phutthai T, Hughes M. 2017. A new species of Begonia section
new genus and species of Rodent (Murinae, Muridae, Rodentia) from Parvibegonia (Begoniaceae) from Thailand and Myanmar. Blumea-
the Khammouan Limestone National Biodiversity Conservation Area Biodivers Evol Biogeogr Plants 62 26-28. DOI:
in Lao PDR. Am Mus Novitates 3497: 1-31. DOI: 10.1206/0003- 10.3767/000651917X695083.
0082 (2005)497[0001:doanga]2.0.co;2. Pinarok NA, Guzman GQ, Alejandro GJ. 2015. Inventory and
Nazarov RA, Pauwels OSG, Konstantinov EL, Chulisov AS, Orlov NL, ethnobotanical study of medicinal plants at Samar Island Natural
Poyarkov NA. 2018. A new karst-dwelling bent-toed gecko Park, Philippines.
(Squamata: Gekkonidae: Cyrtodactylus) from Xiangkhoang Province, Putri IA, Ansari F, Susilo A. 2019. Response of bird community toward
northeastern Laos. Zool Res 39 (3): 202-219. DOI: tourism activities in the karst area of Bantimurung Bulusaraung
10.24272/j.issn.2095-8137.2018.010. National Park. J Qual Assurance Hospitality Tourism 21 (2): 146-167.
Ngo TL, Hölscher D. 2014. The fate of five rare tree species after logging Quang HX, Orlov NL, Ananjeva NB, Johns AG, Thao HN, Vinh DQ.
in a tropical limestone forest (Xuan Son National Park, northern 2007. Description of a new species of the genus Cyrtodactylus Gray,
TOLENTINO et al. – Biodiversity of forests over limestone in the Philippines 1613

1827 (Squamata: Sauria: Gekkonidae) from the karst of north-central Sodhi NS, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW. 2010.
Vietnam. Russ J Herpetol 14 (2): 98-106. The state and conservation of Southeast Asian biodiversity. Biodivers
Quimio J. 2016. Floral composition and timber stock of forest in the Conserv 19 (2): 317-328. DOI: 10.1007/s10531-009-9607-5
Samar Island Natural Park. Ann Trop Res 51: 30-51. DOI: Steinmetz R, Timmins RJ, Duckworth JW. 2011. Distribution and
10.32945/atr3823.2016 conservation status of the Lao Leaf Monkey (Trachypithecus
Rafidah AR, Ummul-Nazrah AR, Hairul MA. 2018. Exacum tenue (francoisi) laotum). Intl J Primatol 32 (3): 587-604. DOI:
(Gentianaceae), a new record from karst limestone in Peninsular 10.1007/s10764-010-9489-0
Malaysia. Gard Bull Singap 70: 103-108. DOI: 10.26492/gbs70 Struebig MJ, Kingston T, Zubaid A, Le Comber SC, Mohd-Adnan A,
(1).2018-10. Turner A, Rossiter SJ. 2009. Conservation importance of limestone
Rafidah AR. 2017. Taxonomy and conservation status of Microchirita karst outcrops for Palaeotropical bats in a fragmented landscape. Biol
(Gesneriaceae) in Peninsular Malaysia. Gard Bull Singap 69: 1-31. Conserv 142 (10): 2089-2096. DOI: 10.1016/j.biocon.2009.04.005
DOI: 10.26492/gbs69 (1).2017-01. Struebig MJ, Kingston T, Zubaid A, Mohd-Adnan A, Rossiter SJ. 2008.
Rahman RA, Kiew R. 2018. Strategy to conserve maximum biodiversity Conservation value of forest fragments to Palaeotropical bats. Biol
of limestone flora in Peninsular Malaysia. J Bot Gard Hortic (16): 57- Conserv 141 (8): 2112-2126. DOI: 10.1016/j.biocon.2008.06.009
66. Suyanto A, Struebig MJ. 2007. Bats of the Sangkulirang limestone karst
Ranlund Å. 2011. Structure and tree diversity of lowland limestone forest formations, East Kalimantan—a priority region for Bornean bat
on Seram Island, Indonesia. Colupsia, EU, Brussel. DOI: conservation. Acta Chiropterol 9 (1): 67-95.
10.1517/14740338.2012.644272 Tan JPC, Kiew R, Saw LG, Ummul-Nazrah AR. 2014. Three New
Restificar, SDF, Day MJ, Urich PB. 2006. Protection of karst in the Species from Gunung Kanthan, a Limestone Tower Karst in Perak,
Philippines. Acta Carsol 35 (1): 121-130. DOI: 10.3986/ac.v35i1.248 Malaysia. Phytotaxa 177 (3): 146-154. DOI:
Riyanto A, Bauer AM, Yudha DS. 2014. A new small karst-dwelling 10.11646/phytotaxa.177.3.2
species of Cyrtodactylus (Reptilia: Squamata: Gekkonidae) from Taylor J, Mate E, Hutchinson R, Eaton J. 2015. Frontiers of the
Java, Indonesia. Zootaxa 3785 (4): 589-599. DOI: Philippines: Eastern Visayas. Birding Asia, Philippines.
10.11646/zootaxa.3785.4.7 Thorburn CC. 2015. The edible nest swiftlet industry in Southeast Asia:
Rösler H, Ziegler T, Vu NT, Herrmann HW, Böhme W. 2005. A new Capitalism meets commensalism. Hum Ecol 43 (1): 179-184. DOI:
lizard of the genus Gekko Laurenti, 1768 (Squamata: Sauria: 10.1007/s10745-014-9713-1
Gekkonidae) from the Phong Nha-Ke Bang National Park, Quang Tuyet D. 2001. Characteristics of karst ecosystems in Vietnam and their
Binh Province, Vietnam. Bonner Zool Beiträge 53 (1/2): 135-148. vulnerability to human impact. Acta Geol Sin 75 (3): 325-329.
Satyanti A, Kusuma YWC. 2010. Ecological study in two quarried Ummul-Nazrah AR, Mohd Hairul MA, Kamin I, Kiew R, Ong PT. 2018.
limestone karst hills in Bogor West Java: Vegetation structure and Vatica najibiana (Dipterocarpaceae), a new species from limestone in
floristic composition. Biotropia 17: 115-129. DOI: Peninsular Malaysia. PhytoKeys (98): 99-106. DOI:
10.11598/btb.2010.17.2.81. 10.3897/phytokeys.98.23903
Saw LG, Chua L, Suhaida M, Yong W, Hamidah M. 2010. Conservation UNDP. 2007. Samar Island Natural Park management plan: June 2006-
of some rare and endangered plants from Peninsular Malaysia. Kew May 2016. United Nations Development Programme, Philippines.
Bull 65: 681-689. DOI: 10.1007/s12225-011-9251-6. Van Der Ploeg J, Van Weerd M, Masipiqueña A, Persoon G. 2011. Illegal
Schilthuizen M. 2000. The evolution and conservation of limestone biotas logging in the Northern Sierra Madre Natural Park, the Philippines.
in Malaysia, with special reference to land snails. In: Leigh M (ed.) Conserv Soc 9 (3): 202-215. DOI: 10.4103/0972-4923.86991
Borneo 2000: Environment, Conservation, and Land. Proceedings of Vermeulen JJ. 1994. Notes on the non-marine molluscs of the island of
the Sixth Biennial Borneo Research Conference. Kuching (Malaysia): Borneo. 6. The genus Opisthostoma (Gastropoda: Prosobranchia:
Borneo Research Bureau, Universiti Malaysia Sarawak, Sarawak. Diplommatinidae), part 2. Basteria 58: 75-191.
Schilthuizen M. 2004. Land snail conservation in Borneo: Limestone Vermeulen J, Whitten T. 1999. Biodiversity and cultural property in the
outcrops act as arks. J Conchol Spec Publ 3: 149-154. management of limestone resources—lessons from East Asia. World
Schilthuizen M, Liew TS, Elahan B, Lackman-Ancrenaz I. 2005. Effects Bank, Washington, DC.
of karst forest degradation on pulmonate and prosobranch land snail Vimal R, Gatiso TT, Mathevet R. 2018. Monitoring in tropical national
communities in Sabah, Malaysian Borneo. Conserv Biol 19 (3): 949- parks : the power of knowledge. Conserv Soc 16 (1): 76-90. DOI:
954. DOI: 10.1111/j.1523-1739.2005.00209.x 10.4103/cs.cs_17_12
Schneider N, Nguyen TQ, Le MD, Nophaseud L, Bonkowski M, Ziegler Wagner J. 2013. Johannes Wagner karst landscapes and karst features in
T. 2014. A new species of Cyrtodactylus (Squamata: Gekkonidae) the Philippines. Selbstverlag, Stuttgart.
from the karst forest of northern Laos. Zootaxa 3835 (1): 80-96. DOI: Wang B, Brand-Miller J. 2003. The role and potential of sialic acid in
10.11646/zootaxa.3835.1.4 human nutrition. Eur J Clin Nutr 57 (11): 1351-1369. DOI:
Schneider N, Nguyen TQ, Schmitz A, Kingsada P, Auer M, Ziegler T. 10.1038/sj.ejcn.1601704
2011. A new species of karst dwelling Cyrtodactylus (Squamata: Watson J, Hamilton-Smith E, Gillieson D, Kiernan K. 1997. Guidelines
Gekkonidae) from northwestern Laos. Zootaxa 2930: 1-21. for cave and karst protection. IUCN Prot Area Prog 1-65. Retrieved
Siler CD, Alcala AC, Diesmos AC, Brown RM. 2009. A new species of from papers2://publication/uuid/62606ABF-255B-4ED0-B444-
limestone-forest frog, genus Platymantis (Amphibia: Anura: 9271DB402F49
Ceratobatrachidae) from Eastern Samar Island, Philippines. Wood PL, Quah ESH, Anuar S, Muin MA. 2013. A new species of
Herpetologica 65 (1): 92-104. DOI: 10.1655/08-040R.1 lowland karst dwelling Cnemaspis Strauch 1887 (Squamata:
Siler CD, Diesmos AC, Linkem CW, Diesmos MLL, Brown RM. 2010. A Gekkonidae) from northwestern peninsular Malaysia. Zootaxa 3691
new species of limestone-forest frog, genus Platymantis (Amphibia: (5): 538-558. DOI: 10.11646/zootaxa.3691.5.2.
Anura: Ceratobatrachidae) from central Luzon Island, Philippines. Wood PL, Grismer LL, Aowphol A, Aguilar CA, Cota M, Grismer MS,
Zootaxa 2482: 49-63. DOI: 10.5281/zenodo.195468 Sites JW. 2017. Three new karst-dwelling Cnemaspis Strauch, 1887
Siler CD, Linkem CW, Diesmos AC, Alcala AC. 2007. A new species of (Squamata; Gekkoniade) from Peninsular Thailand and the
Platymantis (Amphibia: Anura: Ranidae) from Panay Island, phylogenetic placement of C. punctatonuchalis and C. vandeventeri.
Philippines. Herpetologica 63 (3): 351-364. DOI: 10.1655/0018-0831 Peer J 2017 (1). DOI: 10.7717/peerj.2884.
(2007)63[351:ansopa]2.0.co;2 Woxvold IA, Duckworth JW, Timmins RJ. 2009. An unusual new bulbul
Siler CD, Swab JC, Oliveros CH, Diesmos AC, Averia L, Alcala AC, (Passeriformes: Pycnonotidae) from the limestone karst of Lao PDR.
Brown RM. 2012. Amphibians and reptiles, Romblon island group, Forktail 25 (25): 1-12.
central Philippines: Comprehensive herpetofaunal inventory. Check Yong HS, Ng FSP, Lee, EYE. 2004. Sarawak Bau limestone biodiversity.
List 8 (3): 443-462. DOI: 10.15560/8.3.443. Sarawak Museum Journal 59 (6) Spec Issue: 1-411.
Simonsson N, Rodda M. 2009. Hoya platycaulis Simonsson & Rodda sp. Ziegler T, Truong NQ, Schmitz A, Stenke R, Rösler H. 2008. A new
nov. an attractive new Hoya (Apocynaceae-Asclepiadoideae) from the species of Goniuros aurus from Cat Ba Island, Hai Phong, northern
Philippines. Asklepios 106: 13-18. Vietnam (Squamata: Eublepharidae). Zootaxa 1771: 16-30. DOI:
Sodhi NS, Koh LP, Brook BW, Ng PKL. 2004. Southeast Asian 10.5281/zenodo.182143
biodiversity: An impending disaster. Trends Ecol Evol 19 (12): 654-
660. DOI: 10.1016/j.tree.2004.09.006

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