Biodiversity Journal, 2018, 9 (3): 227–236 DOI: 10.31396/Biodiv.Jour.2018.9.3.227.

236

Comparative study on the Anuran Communities (Amphibia

Anura) in Agusan Marsh Wildlife Sanctuary, Philippines

Richel E. Relox1,2* & Fritzie A. Camino2

1
Department of Environmental Science and Technology, College of Science and Mathematics, University of Science and Technology
of Southern Philippines, Cagayan de Oro City, Philippines
2
Department of Biological Sciences and Environmental Studies, College of Science and Mathematics, University of the Philippines
in Mindanao, Mintal, 8000 Davao City, Mindanao, Philippines
*
Corresponding author, e-mail: [email protected]

ABSTRACT The Agusan Marsh Wildlife Sanctuary harbors numerous species of Anurans (Amphibia
Anura) that have highly threatened habitats. The species of anurans were observed in different
vegetation types such as Terminalia forest, sago palms, and rice fields in the Agusan Marsh
Wildlife Sanctuary, Bunawan, Agusan del Sur on May and October 2008. Result showed
abundant, diverse, endemic, and threatened anuran species. Nine species of frogs with 148
individuals were documented. The sago forest had the highest anuran population with 76 in-
viduals (3 species) followed by 41 (5 species) in the Terminalia forest and 31 (3 species) in
the agricultural areas adjacent to sago stands. Of these, 66.7% are Philippine endemics. How-
ever, the remaining 33.3% are threatened by natural habitat conversion. Naturally grown sago
stands are ultimately a habitat for several anurans found only in the Philippine archipelago.
O. laevis and L. leytensis are identified as sago forest indicators. Indeed, their absence or de-
cline in population over time may have detrimental impact on the survival of the sago stands
in the Agusan wetlands. The anuran species are highly habitat specific. Indeed, sago stands
harbor endemic and unique anuran species that need to be conserved and protected.

KEY WORDS Agusan marsh; amphibians; biodiversity; conservation; protection.

Received 27.07.2018; accepted 17.08.2018; printed 30.09.2018; published online 05.09.2018

INTRODUCTION calls (Brown et al., 2008). Therefore, there is no

doubt about future discoveries of new species in
The Philippines has diverse flora and fauna but the Philippines in addition to the present count
are now highly threatened by human activities. To (Taylor, 1923, 1925 as cited by Brown & Gonza-
date, the country has a high percentage of amphib- lez, 2007).
ian endemism (more than 50%) compared to other One of the protected areas in the country, the
groups of wildlife such as mammals, birds, and Agusan Marsh Wildlife Sanctuary, harbors unique
reptiles. Currently, an estimate of 105 species are species of wildlife. This wetland is characterized by
present in the Philippines, which may increase to extensive floodplains and shallow lakes that shrink
160 species considering future conservation stud- and partially dry up from April to October and flood
ies on evolutionary diversification using morpho- from November to late March (RAMSAR, 2003).
logical characteristics, genetic data, and mating It is important not only because of its many ecolog-
228 RICHEL E. RELOX & FRITZIE A. CAMINO

ical functions, from providing habitats to wildlife, Another study in the mountainous areas in Mt.
water cycling and carbon sequestration, to regulat- Sambilikan found and recorded 21 species be-
ing local climate, but also of its economic impor- longing to four families, of which 12 (57%) are
tance to local communities. Not only it holds endemics, while 8 were threatened (Fabricante &
undiscovered and potentially important species, but Nuñeza, 2008). Habitat loss, wildlife hunting, and
it is also the temporary home of migratory birds forest conversion continue to be local threats to
from temperate regions. their survival.
The marsh has different habitat types, such as Thus, this study aimed to determine the recent
the Philippines’ largest Terminalia forest, domi- species composition, diversity, and richness, as
nated by T. copelandii (Frazier, 1999). This type of well as the endemisms and current threats for anu-
forest is an important source of high value timber rans, with reference to three types of vegetation
and other non-wood forest products. Another veg- such as the Terminalia forest, the sago stands, and
etation type is sago palms, which are interspersed the agricultural area in marginal habitats of the
and scattered through the forest. Metroxylon sagu Agusan wetlands. The purpose was primarily to
Rottb., known as sago, serves as a staple food for examine the role of the sago palms as a key habi-
indigenous people in the area during the wet season tat for anuran species and observe the pattern of
or when there arefloods as substitute for rice anuran communities along with habitat modifica-
(Flach, 1997). Ecologically, swamps and wetlands, tions.
home to the sago palms, are among the richest bio-
mes. Sago palms grow in Mindanao and Visayas
dry portions, unlike in the Agusan wetlands. Sago MATERIAL AND METHODS
palms grow individually or in dense clumps
(Mason, 2000 as cited by Palafox, 2006) and are Habitat Characterization
distributed along Southeast Asia, South Pacific,
and South America. However, most of the Termi- The fieldwork was conducted in three selected
nalia forest and the sago palm areas are converted types of vegetation and habitat utilized by amphib-
for agricultural production, especially to rice fields, ians: the Terminalia forest, the sago stands, and the
thus threatening the natural habitats of the fauna. agricultural area of the Agusan Marsh Wildlife
As biological indicators of the health of the envi- Sanctuary located at 8019’0’’N - 125052’0’’E (Figs.
ronment, anurans can be a gauge for disturbed and 1-4). A total of eight sampling sites composed of
undisturbed sites since they have a wide range of five sites in the sago forest with the adjacent agri-
habitats. Some species are highly sensitive to en- cultural areas and three sites of the Terminalia forest
vironmental changes, while others are more toler- in Kaliloan, Bunawan, and Agusan del Sur were
ant to disturbances. carried out on May and October 2008.
In addition, anurans have a broader range of These identified areas have different vegetation.
habitat preferences. By comparing upland studies Some were old-growth forest of Terminalia, while
to other parts of Mindanao (Mt. Hamiguitan other areas have sago stands and the other portion
Wildlife Sanctuary, Davao Oriental), and other of the site is filled with rice fields. They appeared
studies in Lake Sebu, South Cotabato, there is still as patches, ranging from 0.5 ha. to more than 50
an observable high endemism and a certain diver- ha. and serving as buffer zones of the Agusan
sity of amphibians (Ates et al., 2008; Rovillos et marsh. The first, second, and fifth sites were
al., 2008). They are highly specific and diversi- smaller patches, while the third and fourth sites
fied (D=3.66) in aquatic habitats with wide distri- were larger patches. However, the sites were dis-
bution in lowland vegetation. More than 70% of turbed due to slash and burn practices encroaching
the endemism occurred in Mt. Hamiguitan. Few and converting the Terminalia and the sago forests
of these endemic species were threatened. Around into rice fields. The vegetation associated to the
16 species were also counted in Lake Sebu with sago stands are dominated by large trees, vines,
four families. Unsustainable agricultural practices epiphytes, and thick humus cover. The sixth site is
and other anthropological disturbances harm connected to a large timberland, while the seventh
water bodies and low vegetation in Lake Sebu. site is a large patch of the Terminalia forest and
 Comparative Study on the Anuran Communities (Amphibia Anura) in Agusan Marsh Wildlife Sanctuary, Philippines 229

other woody trees. Wildlife hunting, clearings, and animal activity, especially during the night. The
slash and burn practices are prevalent threats in the first major fieldwork began in the sago forest, fol-
eight site of the Terminalia forest. This area is ad- lowed by the agricultural area and the Terminalia
jacent to the sixth site at the border with the Agusan forest. In these sites, flooded forest floor, palm
marsh. foliage, and other low-lying vegetation were ex-
tensively searched for possible amphibian inhab-
Anuran Survey and Its Efficiency itants.
Frogs were collected using bare hands in each
A 100 meters transect line was established microhabitat and placed in plastic containers.
from the edge to the interior of each habitat type, Morphometrics such as snout to vent length
such as the Terminalia forest, sago stands, and (SVL), head length (HdL), hind limb length (HL),
rice fields. Direct counts of amphibians through forelimb length (FL), and tibia length (TbL) were
visual encounter technique and opportunistic sam- measured using a vernier caliper. Distinguishing
pling along the line transects were used to sample morphological characteristics were also noted and
amphibians. Sampling was done from 1800 h to compared to the descriptive data of the Philippine
2200 h per night, from May 10 to 20 and from frogs by Alcala (1982). Man-hours were calcu-
September 24 to October 1, 2008. Transect studies lated by multiplying the number of collectors and
were conducted during periods with the greatest the number of hours spent searching for frogs in

Figures 1-4. Map of the Philippines and location of the eight sampling points in Agusan marsh (Fig. 1) characterized by
three vegetation types such as: Fig. 2: sago stands in water-logged areas. Fig. 3: Terminalia forest. Fig. 4: ricefield, Bunawan,
Agusan del Sur, Mindanao Island.
230 RICHEL E. RELOX & FRITZIE A. CAMINO

each site. Initial records showed six anuran relative abundance of the species. Philippine en-
species in the sago forest and its neighboring demic species and threatened ones were also
habitats, documented in 10 man-hours. This num- counted and analyzed. Current conservation status
ber increased to seven species in 17.5 man-hours based on the International Union for the Conserva-
and climbed up to nine species after 27.5 man- tion of Nature (IUCN, 2017) was determined for
hours. Thereafter, the number of species remained each species. Geographic distribution was digitally
stable up to the last sampling efforts provided. mapped for future monitoring purposes of the sago
There was definitely a sufficient sampling effort areas and its associated vegetation as their habitats.
provided in varied vegetative cover in the Agusan Simpson’s and Shannon-Weaver’s diversity indices,
marsh. richness, evenness and Jaccard’s similarity coeffi-
The number of amphibians for every man-hour cient were calculated to assess the status of the Agu-
in each habitat is used to estimate occurrence and san marsh.

Table 1. Anuran species inhabiting Agusan marsh, Bunawan, Agusan del Sur, Mindanao, Philippines.
Comparative Study on the Anuran Communities (Amphibia Anura) in Agusan Marsh Wildlife Sanctuary, Philippines 231

Table 2. Morphometric data and phenotypic characters used to identify anuran species in the sago forest
and its environs, Agusan marsh, Kaliloan, Bunawan, Agusan del Sur.

Table 2. Biodiversity measurements of anuran communities in Agusan wetlands, Bunawan,

Agusan del Sur, Mindanao, Philippines.
232 RICHEL E. RELOX & FRITZIE A. CAMINO

RESULTS AND DISCUSSIONS The nine species of anurans in the sago forest and
its associated vegetation varies in morphological
Species Composition and Abundance of Anu- measurements (Table 2). Based on the measured
rans in the Agusan Marsh body lengths, the biggest in size relative to other
species are Rhinella marina and Fejervarya vittigera,
The number of captured amphibian species in followed by Fejervarya cancrivora, Polypedates leu-
the sago forest as well as in the adjacent Terminalia comystax, Limnonectes leytensis, Occidozyga laevis,
forest and the agricultural area in the marshland of Philautus acutirostris, Oreophryne anulata, while
Agusan reached 148 individuals with nine species the smallest is Pelophryne lighti. They vary highly
assigned to four families: Ranidae, Rhacophoridae, in morphological characteristics like the possession
Microhylidae, and Bufonidae (Table 1). Among of rough or smooth dorsum, short and long legs, poi-
them, there are the Limnonectes leytensis son glands, and dorsal markings. These are all influ-
(Boettger, 1893), Occidozyga laevis (Günther, enced by the type of life of the anurans in freshwater,
1858), Polypedates leucomystax (Gravenhorst, terrestrial, and arboreal microhabitats.
1829), Philautus acutirostris (Peters, 1867), Fejer-
varya cancrivora (Gravenhorst, 1829), Oreophryne Microhabitats and Species Diversity of Anu-
anulata (Stejneger, 1908), Rhinella marina (Lin- rans in the Agusan Marsh
naeus, 1758), Pelophryne lighti (Taylor, 1920), and
Fejervarya vittigera (Wiegmann, 1835). Previ- The number of aquatic and arboreal species is
ously, only three families of anurans such as generally greater in the Agusan marsh (Fig. 12).
Ranidae, Rhacophoridae, and Microhylidae which In the Terminalia forest, arboreal species were
included eight species such as Fejervarya can- more abundant than aquatic and terrestrial species.
crivora, Pulchrana grandocula (Taylor, 1920), Meanwhile, aquatic species were more in sago
Rana parva Taylor, 1920, Occidozyga laevis, stands compared to the terrestrial inhabitants.
Platymantis dorsalis (Duméril, 1853), Polypedates More terrestrial species dwell in the agricultural
areas compared to the sago and Terminalia forests.
leucomystax, Philautus acutirostris, and Kaloula
Most Occidozyga laevis, Limnonectes leytensis,
conjuncta (Peters, 1863) were recorded (Cabelin,
Fejervarya vittigera, and Fejervarya cancrivora
2007). Other species found in the Agusan marsh
highly preferred the waterlogged habitat of the
were Pulchrana grandocula, Polypedates leu-
sago forest and the adjacent agricultural area
comystax, Kaloula conjuncta, and Occidozyga lae-
rather than the Terminalia forest. Soil availability
vis (Palafox, 2006).
and a stable amount of water support the survival
The most abundant species of amphibians is Oc-
and reproduction of frogs. Tree frogs such as Phi-
cidozyga laevis (47), followed by Limnonectes lautus acutirostris, Pelophryne lighti, and
leytensis (37), Oreophryne anulata (17), Fejervarya Oreophryne anulata live in the Terminalia forest,
cancrivora, Philautus acutirostris, and Fejervarya reaching up to more than 18 meters high and they
vittigera (12), Polypedates leucomystax (7), and are mainly situated in the sago forest. These
Rhinella marina (1) (Figs. 5–10). The highest num- species reside among the leaves and branches of
ber of anurans is found in the sago stands (76) with tall grasses and trees. Polypedates leucomystax
three species such as Occidozyga laevis (41), Lim- and Rhinella marina instead are considered as bi-
nonectes leytensis (34), and Rhinella marina (1). ological indicators of habitat disturbance in the
This is followed by the Terminalia forest (41) with a marsh. The rise of their population number is an
slightly higher number of species (5) such as output of the highest disturbance level occurring
Pelophryne lighti (3), Oreophryne anulata (12), Phi- in the forests.
lautus acutirostris (17), Occidozyga laevis (6), and The species richness of frogs in the Agusan
Limnonectes leytensis (3). The agricultural area is marsh is d=1.68 (Table 3). Amphibian diversity
preferred by three species of anurans, namely: Fejer- values are Ds=0.801 (J’=0.9) and H’=2.637
varya vittigera (12), F. cancrivora (12), and Polype- (ES=0.83) using Simpson’s and Shannon-Weaver’s
dates leucomystax (7), with a total of 31 individuals diversity indices, respectively. There is a higher
(Fig. 11). anuran diversity in this study (H’=1.464) compared
 Comparative Study on the Anuran Communities (Amphibia Anura) in Agusan Marsh Wildlife Sanctuary, Philippines 233

to Cabelin (2007). The sago forest (3.8) had rela- agricultural area and the sago forest and the agri-
tively rich amphibian species compared to the Ter- cultural field. This finding implicates that the sago
minalia (3.23) and agricultural area (2.99). The stands have a greater role in maintaining the diver-
Terminalia forest (Ds=0.71, Es=0.89) adjacent to sity of anurans in the Agusan wetlands as a whole.
the sago stands had significantly higher amphibian Anurans are highly dependent to the sago forest
diversity (Ds) followed by the agricultural area and the timberland. They specialized more on the
(Ds=0.65, Es=0.97) and the sago forest (Ds=0.51, available food resources such as insects (Hy-
Es=0.76). Using Shannon-Weaver’s diversity menopterans, Hemipterans and Orthopterans), fo-
index, the Terminalia forest had consistently the liage, seed, amphibian tadpole, and fish (Palafox,
greatest diversity of amphibians (H’=2.00, J’=0.86) 2006).
compared to the agricultural area (H’=1.54,
J’=3.24) and the sago forest (H’=1.08, J’=0.68). Endemicity and Conservation Status of Anu-
The sago stands served as an alternative habitat for rans in the Agusan Marsh
most amphibian species in the Agusan marsh, since
these areas are also almost immersed in water In the Agusan wetlands, Philippines endemic
throughout the year, similarly to the Terminalia for- frogs are more abundant (66.7%) than non-en-
est. However, some of the water from the forest demics (Fig. 13). The Terminalia forest has the
flow to the rice fields endangering the habitat of highest endemism, followed by the sago forest and
frogs. rice fields.
The composition of anurans between the sago Endemics are abundant in areas with less dis-
and the Terminalia forests (CCj=0.33) is highly turbed vegetation. Naturally grown sago palms
similar. On the contrary, such composition is much and Terminalia trees in water-logged areas are
more dissimilar between the Terminalia and the preferred by anurans. Mindanao endemics are ab-

Figures 5–10. Anuran species found in Agusan marsh, Bunawan, Agusan del Sur, Mindanao. Fig. 5: Fejervarya cancrivora.
Fig. 6: Oreophryne anulata. Fig. 7: Limnonectes leytensis. Fig. 8: Occidozyga laevis. Fig. 9: Fejervarya vittigera. Fig. 10:
Polypedates leucomystax.
234 RICHEL E. RELOX & FRITZIE A. CAMINO

Figure 11. Relative frequency (%) of anurans in three kinds Figure13. Philippine endemics and non-endemics in sago
of habitat in Agusan wetlands, Bunawan, Agusan del Sur, forest, Terminalia forest, and agricultural area, Agusan we-
Mindanao, Philippines. tlands, Bunawan, Agusan del Sur, Mindanao, Philippines.

Figure 12. Microhabitat preference (%) of amphibian spe- Figure 14. Threatened and non-threatened anurans in sago
cies documented in sago forest and its associated vegetation forest, Terminalia forest, and agricultural area, Agusan we-
in Agusan wetlands, Kaliloan, Bunawan, Agusan del Sur. tlands, Bunawan, Agusan del Sur, Mindanao, Philippines.

sent in this wetland. Conversely, non-endemics which began in 2003 (Ibanez & Bastian, 2004), 12
predominated the cultivated areas like the rice species were found and assigned to five families
fields. They proliferate and survive in disturbed and 11 genera. Among them, there were three vul-
habitats. nerable species (Ansonia muelleri, Philautus acu-
Threatened species accounted for 33.3% since tirostris, and Megophrys stejnegeri) and a
their habitats have been exploited by slash and burn threatened species (Limnonectes magnus) docu-
practices and some of them served as subsistence mented.
for human consumption (Fig. 14). In the Terminalia
forest, rather than sago forest and agricultural
areas, threatened species are more abundant than CONCLUSIONS
non-threatened ones. This record may be attributed
to a bigger habitat fragmentation occurring in the Indeed, the Agusan Marsh Willdife Sanctuary
Terminalia forest and the agricultural field than in harbors anurans that are good biological indicators
areas naturally grown with sago. In earlier studies, of habitat disturbance. Anurans exhibited high di-
 Comparative Study on the Anuran Communities (Amphibia Anura) in Agusan Marsh Wildlife Sanctuary, Philippines 235

versity, endemisms, and threatened status in the Cabelin V.L.D., 2007. Amphibian diversity and abun-
Terminalia and the sago forests. Naturally grown dance in Bunawan, Agusan del Sur. Undergraduate
sago stands ultimately serve as a habitat for more Thesis. University of the Philippines Mindanao.
endemic anurans. The aquatic and arboreal species Fabricante K.M.B. & Nuneza O.M., 2008. Anuran
are highly habitat specific. Therefore, the sago species composition, distribution and conservation
stands harbor endemic and unique species and uti- status in Mt. Sambilikan, Diwata range, Agusan del
Sur. In: Proceedings 17th Annual Philippine Biodi-
lizing this habitat for reproduction and survival is
versity Symposium. Human Population Density:
the key to retaining biodiversity in the Agusan
Impacts on Biodiversity. Wildlife Conservation So-
marsh. ciety of the Philippines (WCSP). April 14–17,
2008. Visayas State University, Baybay, Leyte, 43
pp.
ACKNOWLEDGMENTS Flach M., 1997. Sago palm: Metroxylon sagu Rottb. Pro-
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We would like to thank the Philippine Council for and neglected crops 13. International plant genetic
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Development (PCASTRD) - Department of Sci- Frazier S., 1999. RAMSAR sites database: A directory
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(DENR), Protected Areas Management Bureau Ibanez J.C. & Bastian S.T. Jr., 2004. Are sago palm
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Indigenous People (IP) for the collection permit
Project Terminal Report. Biological Sciences and En-
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