Int’l Journal of Advances in Chemical Engg., & Biological Sciences (IJACEBS) Vol.

1, Issue 2(2014) ISSN 2349-1507 EISSN 2349-1515

Abundance, Distribution and Conservation

Status of Reptiles in Agusan Marsh, Bunawan,
Agusan Del Sur, Philippines
1
Meconcepcion M. Ngilangil, 2Lilia Z. Boyles and 2Rainer P. Sularte

 Sanctuary (AMWS) and one of the 128 key biodiversity area

Abstract—The study was concerned about the ecological or (KBA) as well as one of the top 10 priority protected areas in
biodiversity threats among reptiles which are becoming endangered the Integrated Protected Areas System (IPAS). CARAGA’s
or worst extinct. Agusan Marsh Wildlife Sanctuary is one of the species diversity was also high for amphibians (26%) and
most significant and unique wetlands in the Philippines. This study reptiles (62%). The region has 16 endemic amphibians
was the first systematic investigation of reptile species on the marsh. species (42%) and 36 endemic reptiles (53%) (Hilario, 2010).
This study aimed to conduct a systematic study on reptiles in Sago
Still, the region was also not spared from ecological or
swamp and Terminalia forest, Agusan Marsh. The methods used
were a combination of quadrat method, pitfall trap and opportunistic biodiversity threats. Sooner or later, all these species will
during September to December 2013. The study found out that diminish, be endangered and worst, become extinct. Thus, the
eleven (11) species belonging to seven (7) families, with a total of study focuses on reptile species solely.
237 individuals were documented in both sampling sites. Five Reptile species provide a critical role in ecosystems as
species were recorded as Philippine endemic namely; Hydrosaurus predators, and as a group show great diversity in the tropics
pustulatus, Naja philippinensis, Draco quadrasi, Tropidophorus and because of their biological and ecological characteristics,
davaoensis and Tropidophorus misaminius. Among the five endemic it serves as good environmental indicators, providing an
species, Tropidophorus davaoensis and Tropidophorus misaminius excellent starting point for inventorying and monitoring
were Mindanao endemic. Both sampling sites documented high biodiversity.
diversity and more or less even distribution. The association of
Despite a handful of local people dedicated to conservation,
environmental variables with bushes, coconut trees, leaf litter and
tree trunk, selectively logs shows stronger correlation with reptilian the threats to the remaining forest on the mountain are
species such as Eutropis cumingi, Draco quadrasi, and Emoia imminent, leaving an opportunity of perhaps only few years
atrocostata. Despite the exceedingly small land coverage, the Sago to study species and ecosystems and to change the current
swamp and Terminalia forest were confronting threats due to trajectory to better preserve the marsh. Information that will
unprecedented human activities. Conservation action is essential to be gathered from this study can contribute to the existing
protect and preserve biodiversity in the entire Agusan Marsh. scanty knowledge on reptiles especially in Agusan Marsh.
Thus, the study will have an extrapolative value for the
Keywords— Herpetology, Agusan Marsh, microhabitat, conservation management of the reptile community in other
reptilian species, experimental design, Philippines. areas as well. This study endeavors to conduct a systematic
study on reptiles in Sago swamp and Terminalia forest,
I. INTRODUCTION Agusan Marsh that aims to do the following: determine the

P HILIPPINE archipelago was home to a spectacular and

diverse assemblage of amphibians and reptiles. Situated at
the interface between the Oriental and Australian faunal
ecological conditions of Sago Palm (Metroxylon sagu) stands
and Terminalia Forest; determine and compare the species
distribution and abundance between Sago Palm and
zones has now collectively recognized as one of the most Terminalia Forest; determine conservation status of reptiles
important center of herpetofaunal diversity in South East between two vegetation types; lastly, recommend conservation
Asia. Philippine herpetofauna was far richer, the levels of measures between two vegetation types of Agusan Marsh.
endemicity were much higher and the evolutionary history
was far more complex than have been assumed (Diesmos et II. MATERIALS AND METHODS
al., 2002).
By itself, CARAGA or Region 13 (Surigao del Norte, A. The Study Area
Surigao del Sur, Agusan del Norte and Agusan del Sur) has a Agusan Marsh was a vast complex of freshwater marshes
rich ecosystem and hosts a unique community of plant and and water courses with numerous shallow lakes and ponds in
animal species. Agusan Marsh has been declared a Wildlife the upper basin of the Agusan River and its tributaries. It was
located in the province of Agusan del Sur, Northeastern
1
Ngilangil, Meconcepcion M., St. Paul University- Surigao, Surigao City, Mindanao, Philippines which covers an area of 65,806
Philippines, 8400. (Email add: [email protected]).
2
Caraga State University, Ampayon, Butuan City, Philippines, 8600. hectares of which 19,196 hectares was a proclaimed sanctuary

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 Int’l Journal of Advances in Chemical Engg., & Biological Sciences (IJACEBS) Vol. 1, Issue 2(2014) ISSN 2349-1507 EISSN 2349-1515

(Almeria, 2013). It covers a portion of eight municipalities The researcher, along with the local participants and
(Primavera and Tumanda as cited by Almeria & Nuñeza, experts of reptiles conducted two camping trip every day
2013) on which Bunawan was one of the municipalities. (morning and night on the marsh during the research period.
Bunawan, on the other hand, covers several barangays that Each camping trip for every site lasted 4 hours and multiple
includes Sitio Kaliluan where Sago swamp and Terminalia surveys transects (three on average) conducted on each trip
forest were found (Figure1). (Beukema, 2012). Surveys targeted higher elevations where
species endemism would potentially be higher and where
there was less human disturbance. Surveys at different sites
completed within the same time period as much as possible to
minimize differences arising from weather, seasonal, or other
changes and no surveys conducted during vey inclement
weather (Ward, 2012). Each survey quadrat lasted up to 1
hour. Weather permitting, and a day and a night survey done
on the same date, if possible.
Collected samples were identified right away by experts
and were tagged, photographed on the dorsal, lateral and
ventral sides to facilitate scale counts (Beukema, 2011) and
released back into the field. One to two voucher specimens
were prepared especially for species not identified in the field
Fig. 1 Map of Agusan del Sur showing the two sampling area in (Heyer et al, 1994). Those species with unsure identification
Bunawan. were verified using taxonomic keys of Alcala (1986) and
Diesmos et al. (2008) for turtles, Brown and Alcala (1978) as
B. Sampling Sites
modified by Brown et al. (2007,2008) and Zug et al (2007)
Two sampling sites were established as anchored in for gekkonid lizards, Brown and Alcala (1980) and Mausfeld
Almeria & Nuñeza (2013). Sampling site 1, Terminalia et al. (2002) for scincid lizards, Koch et al. (2007) for varanid
Forest was situated at 08° 09.825’ North latitude and 125° lizards. Taxonomy of snakes followed Leviton (1964a; 1964b;
58.044 East longitude. Most of the area was flooded with 1967; 1970b),Ota and Ross (1994) and Utiger et al., (2005).
water and a stream was found within the sampling area. Then, it was sent to experts in herpetofauna, Dr. Arvin
Terminalia forest was a flat primary forest dominated by Diesmos of National Museum of the Philippines and Dr. Rafe
Terminalia copelandii Elm. and Terminalia calamansanay Brown from University of Kansas for identification
Rolfe under Family Combretaceae. Canopy epiphytes, canopy confirmation. Regardless of collection method, if a specimen
vines, understory plants and rare patches of grasses or sedges represented a species previously collected, the specimen was
were found. Fruit trees and mosses of about 10% cover were released. If it is a species not previously collected in the study,
present. Depth of humus cover was about 4 inches with the specimen will be retained and later euthanized by an
alluvium and clay loam soil type. There were few logs; no injection of lidocaine. Specimens were preserved with a 10%
exposed rocks (Almeria & Nuñeza, 2013). formalin solution and later stored in 70% ethanol (Ward,
Sampling site 2, Sago swamp forest was situated at 08° 2012).
09.825’ North latitude and 125° 57.637’ East longitude. It A one-way Anova at 0.05 alpha levels was used to test
was about 300 hectares and has a relatively flat slope. The whether there is any significant difference in the means of
sampling area, constantly flooded with water, has series of diversity in the two habitat types of Agusan Marsh.
brooks and streams. Water level ranged from 9 to 15 inches.
The Sago swamp forest was a secondary growth of D. Microhabitat Analysis
Metroxylon sagu or “sago” under the Palm family Arecaceae. Sample specimens were collected either on a survey or
Pitcher plant was found; moss density was about 40%; leaf opportunistic collection. Notes were taken on the microhabitat
litter was 90% and the depth of humus cover was about one to help determine the conservation needs of each species.
foot with sandy loam soil; fallen logs were minimal caused by Microhabitat descriptions in the filed notes included specific
storm (Almeria & Nuñeza, 2013). details such as physical characteristics (grass, humus, bare
soil, stream banks, on the ground, etc.) and associated
C. Species Inventory
vegetation (Ward, 2012), including the species name when
To achieve the inventory of reptile species, specimens was possible. The descriptions were grouped into more general
collected in three ways: survey transects, pitfall trap method categories such as leaf litter, rotting log, tree trunk, tree
and opportunistic collection. These techniques employed branches/ leaves, ground cover vegetation and others (Neal,
intensive sampling of arboreal, surface and subterranean 2007). Because many specimens were opportunistic
strata in the chosen sites (Almeria & Nuñeza, 2013). Two collections, human-made objects (such as houses or
transect line (1km) with three quadrats of about 20x20 m was equipment in people’s yards) and human- maintained
laid down randomly in each sampling site with 20m away vegetation (such as farms, gardens and roadsides) were used
from each quadrat. It was conducted last September to as microhabitat categories (Kati, 2007).
December 2013.

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III. RESULTS AND DISCUSSION in sampling station 1.1. Naja philippinensis shows its
The Sago Palm area was a secondary forest dominated by apparent association with environmental variable with road
Metroxylon sagu under the Palm family Arecaceae and it was kills, in sampling station 1.1
about 3 hectares with a vegetation type composed primarily of
tall grass, vines, shrubs, and epiphytes. There were other trees
spotted in the area like Lanipao, Wango, Manga Pajo,
Kabihid and Libas. While few of Baas, Panabog, Dagahit and
Ferns (Pako) were also noted. The observed bed floor of Sago
Palm was watery with the presence of rotten logs and leaf
litters while the soil type was peat lands (Figure 2). Peat lands
were wetlands with a thick water-logged organic soil layer
(peat) made up of dead and decaying plant material as
documented by Santillan et al (2012). The distance from the
sampling site to anthropogenic clearing of a large scale rice
plantation and human settlement was about 50 meters. An
abandoned slash and burn farm was observed at the periphery
of the sampling site as also noted by the study of Almeria &
Nuñeza (2013).
Terminalia Forest was a flat primary forest dominated by
Terminalia copelandii under Family Combretaceae. The
vegetation type of this area was composed of tall grass, vines,
shrubs, and epiphytes. Tree taxa of Terminalia forest were
primarily composed of Manga Pajo, Maymayan, Lanipao,
Katumbawon, Kapi-kapi, Salumbayan, Tayapok and
Hambabawod. Some of the trees produce fruits that were
eaten by endemic birds in the area. Dominate grasses found in
the area include Baas, Bagahit, Bakong, Tambo, Muti-muti
and Bangiba. While, ground cover plants such Fern and Fern-
allies, Pitcher plant, and Badyang were recorded. Most of the Fig. 2. Natural habitats on ground dwelling (A), leaf litter (B)
area was flooded with water and a small stream was found and rotten sago and log trunks (C)
within the sampling area. Rotten logs, left litters and tree
holes were documented but no exposed rocks. Soil type was
clay loam and presence of depth humus cover was also noted.
The distance from the sampling site to anthropogenic clearing
and human settlements was approximately 50 meters. Slash
and burn can be observed few meters away from the sampling
site.
Environmental parameters in the two vegetation types of
Agusan Marsh were recorded such as ambient temperature;
wet temperature was 31°C while dry temperature was 30°C.
The sky during the day was partly cloudy but varied every day
during the fieldworks. Relative humidity was 79% while Fig. 3. Ordination of species and environmental variables in the
vapour pressure (mmHg) 23.75 mm while the dew point first two canonical axis from CCA scores.
temperature was 42.6 dc. In addition, rainfall (mm) during
the sampling period was 376.7 and the average wind speed Moreover, the clustering of species and environmental
variables with swampy areas and small streams shows strong
(mps) was 002 (Data taken from Hinatuan Weather Station) .
association with Cuora amboinensis, this can be explained
Habitat quality was a measure of the importance of habitat
that this species prefers this specific environment. With
type in maintaining a particular species (Van Horne, 1983).
reference to study of Hofer et al., 2000, that response of
In the CCA ordination (Figure 3) sampling site 1.1 and
reptiles to streams shows pronounced preference as it gives
1.2 shows particular environmental patterns. The association large CCA score, thus its abundance affects stronger relation
of environmental variables with bushes, coconut trees, leaf to its environment. Species that negatively correlates small
litter and tree trunk, selectively logs shows stronger streams Tropidophorus misaminius and Broghammerus
correlation with reptilian species such as Eutropis cumingi, reticularus, this species were given small weight in the CCA.
Draco quadrasi, Emoia atrocostata. On the upper- right
quadrat, Hydrosaurus pustulatus, Tropidophorus davaoensis
shows its stronger relation in the human maintain vegetation

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Species Distribution and Abundance TABLE I

SPECIES DIVERSITY AND EVENNESS OF REPTILES IN THE TWO SAMPLING
Sago swamp and Terminalia forest both documented 11 SITES IN AGUSAN MARSH.
species of reptiles belonging to seven (7) Families Agamidae, SAGO PALM TERMINALIA FOREST
Elapidae, Gekkonidae, Geomyididae, Pythonidae, Scincidae Taxa_S 11 11
Individuals 113 124
and Colubridae, including, 7 lizards, 3 snakes and 1 turtle Dominance_D 0.1306 0.1206
Simpson_1-D 0.8694 0.8794
Shannon_H 2.16 2.196
Evenness_e^H/S 0.7886 0.8171
A slightly higher diversity was recorded in the Terminalia
forest (H’ = 2.196) compared to Sago swamp forest (H’ =
2.16). This implies that Terminalia Forest had rich number of
number of individuals may be due to more favourable habitat
types for herpetofauna such as close canopy of trees with tall
grasses, watery bed floor, adjacent to herbaceous-swamp and
suitable climatic conditions such temperature. Rainfall
Fig. 4 The Eleven (11) documented species namely (L-R); (378mm-528.8mm) was high in Terminalia making the area
Hydrosaurus pustulatus, Emoia atrocostata, Hemidactylus frenatus, more productive. Floodplains and large woody debris in the
Broghammerus reticularus, Cuora amboinensis, Draco quadrasi, Terminalia forest were abundant as cited by Almeria &
Eutropis cumingi, Tropidophorus misaminius, Tropidophorus Nuñeza, 2013. Active floodplain, vegetated islands and large
misaminius, Boiga dendrophila divergens, and Naja philippinensis. woody debris are important, directly and indirectly, in
A total of 237 individuals were documented, in the Sago maintaining both habitat and herpetofauna diversity and
swamp forest (113) and Terminalia forest (124) for the whole density (Klaus et al., 2006 as cited by Almeria & Nuñeza,
duration of the study. The three techniques namely, survey 2013).
transects, pitfall trap method and opportunistic collection On the other hand, the computed species evenness in the
were employed in the study. Pitfall traps sampled a lower two habitat types, Sago Palm (0.7886) and Terminalia Forest
number of individuals and species than the other two (0.8171) was moderate that might be for the reason of having
methods, but was more efficient for sampling one particular almost the same parameters such seasonal variation, elevation
species, the Emoia atrocostata. In a study of Almeida-Gomes range, habitat type and availability of foods. Combination of
et al., (2008) at Atlantic rainforest area in Rio de Janeiro factors that favored speciation in the past, including
State, pit-falls also seemed not efficient than the other fluctuating sea levels (created habitats with equable climatic
methods. Most opportunistic collections were contributed by conditions) , complex geologic (tectonic) events (favoring
people in the locality or found while on camping trips but not creation of many microhabitats) and promoting geographic
during the actual survey transects. The Sago plants barriers to population mixing made it a reason for high
(Metroxylon species) with a distinctive features of elongated species richness and high endemism (Heaney 1985; Sodhi et
large leaves that are provided with sharp spiny thorns that al. 2004; Brown & Diesmos2009).
accumulate on the forest floors of the Sago palm forest as Conservation Status
cited by Almeria & Nuñeza, 2013 made it difficult for the
researchers and local guide to penetrate on the area; only The researcher documented species that were under
highly adapted or tolerant species may be able to cope with conservation status, including 2 vulnerable/ decreasing, 7
this condition (Miller et al., 2001 as cited by Almeria & least concern/stable and 2 near threatened/decreasing Five
Nuñeza, 2013). species named Hydrosaurus pustulatus, Naja philippinensis,
Terminalia forest was a watery area dominated with tall Draco quadrasi, Tropidophorus davaoensis and
grasses and trees and the canopy of trees are very close from Tropidophorus misaminius were documented living only
one another. The adjacent area of Terminalia forest was rice (endemic) in the Philippines based on the IUCN 2007.
fields where insects and other micro-pests lived, this insects Among the 5 endemic species, Tropidophorus davaoensis and
and micro-pests serves as food. In addition, frequent rainfall Tropidophorus misaminius were considered as Mindanao
increase the density of food resources of reptiles, probability endemic (Amoroso, 2000 as cited by Beukema, 2011). With
of breeding, larval survival and juvenile recruitment (Gray et reference to the 2007 IUCN Red Data List, the researcher
al., 2004, as cited by Almeria & Nuñeza, 2013) gave a identified three endemic species with Least Concern/stable
contributing factor of species abundance. On the other hand, conservation status; these include Draco quadrasi,
Terminalia forest was the most extensive area left in the Tropidophorus davaoensis and Tropidophorus misaminius,
Philippines on which historical records indicate that this kind while Hemidactylus frenatus, Broghammerus reticularus and
of forest was fairly common in marshes in the country. Emoia atrocostata which are not endemic were also in Least
However, most of the Terminalia forest has been cleared; Concern status. While Naja philippinensis and Boiga
hence, it was particularly vulnerable to clearing (RAMSAR, dendrophila divergens were near threatened and also
2000) decreasing. Killings of snakes accidental along the road were
observed. Ashley and Robinson (1996), as cited by Sharma

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(2011), observed that the road-kills of reptile are a major Hence, extraction of forest resources by the villages of the
cause of mortality for a wide variety of taxa. Hydrosaurus forest perimeter was leading to overexploitation, and
pustulatus and Cuora amboinensis were identified as enhancing extent of disturbances (Surasinghe & Jayaratne,
vulnerable and likely decreasing. Raising of Cuora 2006). On the other hand, Kaingin or Slush and Burns
amboinensis for pet and food consumption were observed in (Figure 5C) in the area were noted during our field sampling.
the locality. Harvesting of herpetofauna through illegal trade This not only destroys the habitats but also directly kills the
and unsustainable consumption was probably the biggest reptile and amphibian species. Moreover, burning would
threat other than habitat destruction and alteration as cited by hinder the development of the secondary successions. In
Neal (2007). (Zug et al., 2001). certain situations, fire spreads even into the core-forest areas
Though, this study accounted only 11 (17.8%) species causing significant degree habitat destruction (Surasinghe &
with 2 (5.5%) were endemic (Tropidophorus davaoensis and Jayaratne, 2006). With the ongoing disturbances in the
Tropidophorus misaminius) this does not exactly indicate Agusan Marsh, it appears that the endemic species are more
reptile species decline in Agusan Marsh as the surveys were at risk (Almeria & Nuñeza, 2013). Poynton et al., (2007), as
encountered only for four months. This decrease could be due cited by Almeria & Nuñeza, 2013), reported that the
to either samples being missed, especially if individuals are uniqueness of the species combined with their evident
small in size and residing in the clumped leaf litter, species vulnerability to disturbance make them a subject for
being well camouflaged, or the ability of individuals to escape particular conservation.
even before they were noticed (Ates- Camino et al., 2010). In The researcher come up with these policies for
addition, the researcher supposes that the swifter nature of conservation management; first, a legal framework must be
reptiles compared to amphibians and their limited of absence established to prevent disturbances, especially encroachments
of vocalization may have account for their rarity of capture. and forest-resource overexploitation and the law enforcement
should be functional to take legal action against violation of
Environmental Threats and Conservation Management
rules; second, a pilot project was also need to carry out to
Despite the exceedingly small land coverage, the Sago monitor the population status of reptile species and the biotic
swamp and Terminalia forest was confronting threats due to and anthropogenic factors affecting those; third, the
unprecedented human activities. Today, the major threat of landowners of the nearby private agricultural lands must be
reptile species in Agusan Marsh was the on-going conversion encouraged to adopt agroforestry practices. This will allow
of Sago and Terminalia Forest into agricultural land (Figure establishment of small populations of herpetofauna that can
5A,B). Local residents such as the Manobo have cleared function as subpopulations. Later on, such small populations
portions for corn, vegetable and rice production. The will interbreed with the main populations in the reserve and
agricultural chemicals and pesticides used in corn, vegetable will create metapopulations; lastly, forest management should
and rice production results in secondary problems for target the maintenance of the open forest structure with low
herpetofaunal communities with the mass killing of insect bush under growth, to favor the diversity of terrestrial reptiles
communities, which was an integral component of their food (Surasinghe & Jayaratne, 2006).
niche (Bishop and Gendron, 1998; Somaweera, 2001;
Bambaradeniya, 2001 as cited by Surasinghe & Jayaratne IV. CONCLUSION
,2006). Besides, there was a tendency for bioaccumulation
Sago plam and Terminalia forest still harbour unique
and biomagnification of the pesticides to occur through food
community of reptilian species regardless of the on-going
webs (Moriarty, 1975; Feleers et al., 2004 as cited by
anthropogenic activities in the area like Kaingin, conversion
Surasinghe & Jayaratne , 2006 )
of lands to agriculture and harvesting of species for pet trade,
medicine, and food consumption in the rest of Agusan Marsh
are any indication that the clock was ticking on this unique
and valuable ecological refuge. Data from this study suggest
that reptiles in Terminalia Forest and Sago Palm need urgent
protective measures and management including other wildlife
faunal species in the area. Protection and conservation
Fig. 5On-going anthropogenic activities inside Sago Palm and priorities of the reptilian species and long-term monitoring
Terminalia Forest of Agusan Marsh. programmes within the Sago palm and Terminalia forest of
Agusan Marsh will be closely monitored by our local and
Cutting and clearing of Terminalia trees for charcoal provincial government and some non-government
making and firewood production as well as harvesting organizations (NGOs) in the country.
(hunting/gathering) of wildlife vertebrates for food
consumption (wild pig capture) were the present livelihood of ACKNOWLEDGEMENT
some local residents in the area. Like the species Cuora
amboinensis on the study of Brown et al., 2012, it was heavily The author wishes to express her sincere thanks to all
hunted for food, curiosities, pet trade and traditional medicine individuals who contributed their valuable assistance in the
which were also observed in the locality of Agusan Marsh. preparation and completion of this study, especially to Dr.

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Arvin Diesmos of National Museum of the Philippines and [24] Newmark, W. D., 1998. Forest area, Fragmentation and loss in the Eastern
Arc mountains: implications for the conservation of biological diversity.
Dr. Rafe Brown from University of Kansas for identification [25] Nguku J.K., 2009. Distribution, diversity and population status of
confirmation. To the St. Paul University- Surigao especially herpetofauna in Lower Tanariver forests, Kenya.
to Sr. Rosanne Mallillin, SPC for providing her with moral [26] Oliveros C.H., Ota H., Crombie R.I., Brown R.M., 2011. The
Herpetofauna of the Babuyan Islands, northern Philippines.
and financial support during her study and for the chance and [27] Petrov B., 2007. Amphibian and reptiles of Bulgaria: Fauna, vertical
effort in sending her in the IICBE conference. distribution, zoogeography and conservation.
[28] Poynton, J. C., Loader S. P., Sherratt E., Clarke, B. T., 2007. Amphibian
diversity in East African biodiversity hotspots: altitudinal and latitudinal
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