Species Diversity,Distribution,and Microhabitats of Anurans on Mt.Kalo-Kalo of the Mt.Kalatungan Range Natural Park,Bukidnon,Philippines

Von Carlo P.DELA TORRE and Olga M.NUNEZA

1 Department of Biological Sciences and Environmental Studies,University of the Philippines Mindanao,Mintal,Tugbok District,Davao City 8022,Philippines

2 Wildlife-Human Interaction Studies,Ecological Research,and Biodiversity Conservation Laboratory,University of the Philippines Mindanao,Mintal,Tugbok District,Davao City 8022,Philippines

3 Department of Biological Sciences and Biodiversity Laboratory,Premier Research Institute of Science and Mathematics,Mindanao State University-Iligan Institute of Technology,A.Bonifacio Ave,Iligan City 9200,Philippines

Abstract Anurans are considered good indicators of habitat quality due to their bi-phasic life mode,limited dispersal abilities,and sensitivity to environmental changes brought about by habitat fragmentation,pollution,climate change,and emerging infectious diseases.This study aimed to determine species diversity and local distribution of anurans in lower (1000-1400 masl) and upper (1400-1600 masl)montane forests on Mt.Kalo-Kalo of the Mt.Kalatungan Range Natural Park,Central Mindanao,Southern Philippines by employing standard sampling techniques for amphibians.We recorded a total of 251 individual anurans,representing 12 species during a brief recent study period.Mt. Kalo-Kalo’s upper montane forest has a higher diversity index (H’=1.276)than the lower montane forest (H’=0.851).Despite the very low diversity indices,the level of endemism of anurans was 100% where ten of the recorded species are Mindanao Faunal Region endemics and an additional two species are Philippine endemics.Ansonia muelleri exhibited the highest local abundance and individuals of this species which constituted 73% of individual anurans observed.Most of the species encountered prefer terrestrial and aquatic microhabitats,specifically on the rocks and bank substrates along the rivers and streams.Three species of anurans (Philautus acutirostris,P.poecilius,and Rhacophorus bimaculatus) were strictly found in arboreal microhabitats.Limnonectes magnus and A.muelleri have overlapping microhabitats.Results indicate that for such a short survey and modest sampling effort,the lower and upper montane forests of Mt.Kalo-Kalo support high endemism of anuran species suggesting that conservation efforts continue to be a priority in this unique protected area.

Keywords conservation,endemic,indicator species,montane forest,protected area

1.Introduction

The herpetofauna of the Philippine Archipelago is taxonomically diverse and species-rich (Inger,1954;Alcala,1986;Brown

et al

.,2001,2009;Brown and Siler,2013) with a total of 112 Philippine amphibians (84% endemic) and 368 (66%endemic) Philippine reptile species (Diesmos

et al

.,2015;Uetz

et al

.,2020).These high levels of diversity and endemism have been continuously reaffirmed by biogeographical hypothesis testing,based on the Pleistocene Aggregate Island Complex(PAIC) model (Heaney,1985;Brown and Diesmos,2002,2009;Esselstyn and Brown,2009;Lomolino

et al

.,2010;Siler

et al

.,2010).Employing this perspective,nine herpetological subregion Pleistocene Aggregate Island Complexes (PAICs) have been recognized as centers of biological diversity and endemism(Batanes Island Group,Babuyan Island group,Luzon PAIC,Mindoro Island,Romblon Island Group,Palawan PAIC,Visayan PAIC,Mindanao PAIC,and Jolo-Tawi-Tawi PAIC),each supporting unique herpetofaunal communities (Brown

et al

.,2001;Diesmos and Brown,2011;Brown and Siler,2013;Diesmos

et al

.,2014).The faunal regions of the Philippines have been described by Heaney and colleagues based on more than 40 years of research (Heaney 1986,1998,1999,2000,2004;Heaney

et al

.,1990,1998,2005).Past efforts to document the natural history and biology of amphibians and reptiles by herpetologists and biogeographers have revealed the herpetological and conservation importance of the Philippines (Brown

et al

.,2008,2012,2013;Diesmos and Brown,2011;Diesmos

et al

.,2015;Sanguila

et al

.,2016).However,complete knowledge of the ecology and distribution of many species is still lacking,which is a challenge to effective conservation planning and species-specific intervention(Margules and Pressey,2000).Several studies have been conducted to describe the species diversity and distribution of the herpetofauna in the Philippines,including forested mountains of the Luzon PAIC (Mcleod

et al.

,2011;Devan-Song and Brown,2012;Brown

et al.

,2012;Brown and Siler,2013;Gojo Cruz

et al

.,2018),the Babuyan Island Group (Oliveros

et al

.,2011),Romblon Island Group (Siler

et al.

,2012),Panay Island (Ferner

et al

.,2000;Gaulke,2011),Cebu Island (Supsup

et al

.,2016),and Leyte Island (Aureo and Bande,2017).On Mindanao Island,herpetological surveys are increasing in frequency (David

et al.

,2006;Delima

et al.

,2007;Nuñeza

et al.

,2010,2014,2015,2017;Beukema,2011;Almeria and Nuñeza,2013;Warguez

et al.

,2013;Sularte

et al.

,2015;Calo and Nuñeza,2015;Plaza and Sanguila,2015;Sanguila

et al

.,2016;Toledo-Bruno

et al

.,2017;Vidal

et al

.,2018;Delima-Baron

et al

.,2019).However,large areas of Mindanao are still unexplored (Heaney

et al

.,2006;Peterson

et al.

,2008;Siler

et al

.,2009;Beukema,2011;Sanguila

et al

.,2016),and many new species are still being described (Brown

et al.

,2009;Siler

et al.

,2009).Mindanao is located in the southern part of the Philippine archipelago.It is considered a unique island for biogeographers and conservationists to study impacts of evolutionary diversification in archipelagos,since it is home to faunal elements that are both of Sundaic and Sulawesian origins(Esselstyn

et al

.,2009;Setiadi

et al

.,2011).In the late twentieth century,the southern portions of the archipelago have been viewed to be more diverse than the northern portions of the archipelago in terms of faunal diversity (Inger,1954;Leviton,1963;Brown and Alcala,1970),in the sense that the northern islands are perceived as the ends of colonization routes and the extreme endpoints of dispersal for Sundaic faunal elements(Huxley,1868;Dickerson,1928;Inger,1954,1999;Myers,1962;Diamond and Gilpin,1983;Brown and Guttman,2002;Jones and Kennedy,2008).However,recent faunal surveys in the northern portions of the archipelago showed high species diversity and endemism (Linkem

et al

.,2010;Heaney

et al

.,2011;Brown

et al

.,2013).Hence,northern portions of the archipelago may be more diverse than generally appreciated (Heaney

et al

.,2010,2011;Balete

et al

.,2011;Duya

et al

.,2011;Siler

et al

.,2011;Brown

et al

.,2013;Diesmos

et al

.,2015).Mt.Kalatungan Range Natural Park (MKaRNP) is located in the central section of Mindanao Island,Bukidnon Province.It was designated as a protected area on 5 May 2000,under Proclamation 305. Mt.Kalatungan Range Natural Park is under the administrative jurisdiction of the Department of Environment and Natural Resources (DENR),through the Protected Area Management Board (PAMB) and administered in accordance with the provisions of the National Integrated Protected Areas System (NIPAS) Act of 1992 (Official Gazette of the Republic of the Philippines,2000).Mt.Kalatungan Range Natural Park covers an area of approximately 35,139.230 hectares of which 21,247.730 hectares consist of the strict protected area whereas 13,891.500 hectares make up the buffer zone.Its current status is considered threatened by habitat fragmentation.Efforts to assess the anuran species diversity and distribution in MKaRNP have been done previously by Warguez

et al

.(2013) and Toledo-Bruno

et al

.(2017).However,they were at different sampling sites,elevations,sampling efforts,and seasons.A large part of the mountain range on MKaRNP is still in need of biodiversity assessment of anurans(Warguez

et al

.,2013;Toledo-Bruno

et al

.,2017).One of these mountains in MKaRNP is Mt.Kalo-Kalo which is located at the southeastern part of the MKaRNP (Figure 1),with a peak of 1730 masl.The climate falls within Type III,characterized as having a short dry season lasting only from 1 to 3 months.The highest amount of rainfall occurs in June while March is the driest month (Toledo-Bruno

et al

.,2017).The Philippines is considered one of the most imperiled of the global biodiversity conservation hotspots because of high levels of endemism and alarming rates of destruction of fauna and flora brought about by overexploitation,deforestation,habitat degradation,climate change,and pollution (including biological pollution),among other factors (Heaney and Mittermeier,1997;Mittermeier

et al

.,1999;Catibog-Sinha and Heaney,2006;Mittermeier

et al

.,2011).From originally ＞85%forested,the archipelago now retains only 4%-8% of original forest cover (Catibog-Sinha and Heaney,2006).The Philippines needs at least 52% of total land area covered by forests to maintain a healthy and stable ecosystem (DENR,1989).However,the country has already reached the point below this threshold from about 68% forest cover in 1876 to 24% in 2003(Fernando,2005).Anurans are considered good indicators of habitat quality due to their bi-phasic life mode and sensitivity to environmental changes.They are notoriously affected by ha bitat fragmentation and logging.These environmental changes elicit changes in microclimatic variables,which manifest as a disturbance gradient in the habitat structure which is impactful to amphibians due to their limited dispersal capabilities (Alcala and Custodio,1995;Hampson,2001;Davic and Welsh,2004;Bickford

et al

.,2010;Heatwole and Wilkinson,2012;Jiang

et al.

,2016).Anurans are one of the severely threatened faunal groups within the Philippines,with one“Critically Endangered”(

Platymantis insulatus

),one“Endangered”(

Platymantis spelaeus

),and 21“Vulnerable”species (Philippine Red List Status,2019).The Philippine Archipelago has a significant and an increasing trend of forest cover loss exceeding that anywhere else in the planet (Sodhi

et al

.,2004) with forest loss of at least 2.61 km/yr (Fallarcuna and Perez,2016).This may threaten anuran diversity,so new survey efforts on anurans are desirable and justified.Here we provide species accounts and determine the species diversity,distribution,and microhabitats of anurans in the upper and lower montane forests on Mt.Kalo-Kalo of the Mt.Kalatungan Range Natural Park.

Figure 1 Center:Map of the Mt.Kalatungan Range Natural Park (MKaRNP).Lower Bottom Left:Map of the Philippines.Lower Bottom Right:Map of the Mt.Kalo-Kalo in MKaRNP showing the two sampling sites in the lower montane (1000-1400 masl) and upper montane (1400-1600 masl) forests.

2.Materials and Methods

2.1. Study Sites

Sample collection was done in the lower montane forest at 1000-1400 meters above sea level (masl)(Figure 2) and upper montane forest (1400-1600 masl) (Figure 3),that is,from submontane to montane forest of Mt.Kalo-Kalo,Mt.Kalatungan Range Natural Park,Sitio Bauhon,Barangay Dagumbaan,Municipality of Maramag,Bukidnon Province,Philippines which is geographically located at 7°54’27”N,124°54’32”E (WGS84) (Figure 1).The distance between the upper and lower montane forests was ca 2-3 kilometers.Delineation of upper and lower montane forests was based on vegetation types of sampling areas (Toledo-Bruno

et al

.,2017). Descriptions of the habitats were based on the Habitat Description Form(HDF) (National Research Council,1981).

Site 1

Lower Montane Forest (7°54’6”N,124°54’42”E):has an altitude of 1000-1400 masl (Figure 2) characterized by tall and big“Ulayan”(

Lithocarpus

spp.)emergent trees up to 45 m tall and 90 cm diameter at breast height (dbh).“Repetek”(

Kokoona ochracea)

is the canopy tree with a dbh of 84 cm and height of 40 m.Wild orchids,Bird’s nest fern,and vines are observed.

Thespesia populnea,Syzgium

spp.,

Agathis philippinensis

,

Cof fea arabica

,

Sphaeropteris

spp.,

Alsophila

spp.,Pandanaceae

,

and Araceaeare observed in moderate numbers.Some of the trees observed are covered with mosses and ferns.The ground is covered with moderately dense leaf litter of 2-5 layers.

Site 2

Upper Montane Forest (7°55’34”N,124°54’43”E):has an altitude of 1400-1600 masl (Figure 3) characterized by“Ulayan”(

Lithocarpus

spp)as emergent trees with a dbh of 70 cm and height of 40 m.and“Tampoy”(

Syzygium

spp.) canopy trees with a dbh of 61 cm and height of 37 m.

Thespesia populnea

,

Agathis philippinensis

,

Phyllocladus hypophyllus

,

Sphaeropteris

spp

.

,

Alsophila

spp.,

Colocasia esculenta,

and

Callamus deeratus

are observed in moderate densities in the montane forest.Trees are mostly covered with mosses and epiphytic plants like ferns.The ground is covered with 3-7 layers of leaf litter.Generally,the montane forests in the Philippines are characterized by the presence of the

Lithocarpus

spp.,

Syzygium

spp.,and gymnosperms such as

Agathis philippinensis

and

Phyllocladus hypophyllus

,including tree ferns of the family Cyatheaceae and Dicksoniaceae (Whitford,1991;Gruezo,1997;Buot and Okitsu,1998;Fernando

et al

.,2004;Amoroso

et al

.,2011).Microhabitats in this study were divided into four categories according to the microhabitat types of Gonzales and Dans(1994),namely:Type I:Arboreal microhabitats as characterized by clumps of moss and other bryophytes and epiphytic plants such as orchids,ferns,and vines/climbers present on trees or above the ground (Figure 2);Type II:Leaf-axils as characterized by water-filled axils ofAraceae,Pandanaceae,Musaceae,and Cyatheaceae(tree ferns) (Figure 4);Type III:Vertical stratum as characterized by tree holes and similar crevices in the main branches approximately along the middle stratum of the forest,including tree bark and buttresses (1-10 m high) (Figure 5);and lastly,Type IV:Substrate level or ground litter as characterized by rocks along the streams,tree stumps,burrows,fallen logs or tree fall,and leaf litter (Figure 6).

2.2. Sampling Technique

Field surveys were conducted during the rainy season from 29 April-30 May 2019,for a total of 32 field-days and 896 person-hours.Anurans were collected using random sampling,visual encounter techniques(Plaza and Sanguila,2015),and cruising techniques (Nuñeza

et

al

.,2017).Cruising techniques were conducted during diurnal(700-1000) and nocturnal (1800 -2200) times,employing an opportunistic approach,such as capture by hand.Standard collection and specimen preservation techniques were utilized(Heyer,1994;Simmons,2002) and the collected specimens were photographed alive.Notes on microhabitat preferences and coloration were taken.After capture,one to two voucher specimens under Wildlife Gratuitous Permit No.R10 2019-48 were processed immediately in the field station and euthanized with denatured alcohol by injecting a small amount in the vent of each specimen (Heyer,1994;Simmons,2002).Digital vernier calipers and Pesola® spring balances were used to obtain the measurements and body weight of each specimen,respectively.Measurements include snout-vent length (SVL),head width(HW),head length (HL),tympanum width (TW),eye diameter(ED),forelimb length (FL),and hind limb length (HiL) (Watters

et al

.,2016).These measurements and body weight were taken for accurate identification of anurans.Initial identification of specimens followed Inger (1954),Alcala and Brown (1998),Nuñeza (2012),Diesmos

et al

.(2015),and Sanguila

et al

.(2016).Once identified,most specimens were returned to the wild.Representative samples were initially fixed in 10% formalin in the field and were later transferred to 70% ethanol at the Mindanao State University -Iligan Institute of Technology,Premier Research Institute of Science and Mathematics,Biodiversity Laboratory.Accounts for each species are provided and identifications validated by Dr.Rafe M.Brown of the University of Kansas,Biodiversity Institute,Lawrence,Kansas,United States of America.Determination of socioeconomic importance of anurans and potential threats to the anurans and their habitats was based on key informant interviews in a local community and on direct observations.Three respondents in the community of Sitio Bauhon,Barangay Bagumbaan,Maramag,Bukidnon,who are knowledgeable of anurans and have at least ten years of residency in the area,provided information such as abundance and threats to anurans at the sampled sites.

2.3. Data analysis

Paleontological Statistics Software (PAST)version 3.06 (Hammer

et al

.,2001) was used to determine biodiversity indices.Biodiversity indices were used to analyze the data gathered.These indices were the relative frequency,richness,diversity,evenness,and dominance.Relative species frequency refers to how common or rare a species is relative to others in a given location or community (Magurran,1988;Iskandar and Kotanegara,1993).

3.Results

Figure 2 Characteristic appearance of the lower montane forest and Type I microhabitat.

Figure 3 Characteristic appearance of the upper montane forest.

3.1. Species Composition and Abundance

Twelve species of anurans were documented in the upper montane forest of Mt.Kalo-Kalo on MKaRNP.Of these species,10 are Mindanao Faunal Region endemics and two are Philippine endemics.There are three species in the family Rhacophoridae,two species in Megophryidae,Ranidae,and Dicroglossidae,and one species in Bufonidae,Cetatobatrachidae,and Microhylidae (Table 1).

Ansonia muelleri

(Bufonidae) was the most abundant species with 70.13% relative frequency followed by

Rhacophorus bimaculatus

(Rhacophoridae)(6.25%),

Megophrys stejnegeri

(Megophryidae)(4.86%),

Leptobrachium lumadorum

(Megophryidae)(4.86%),

Staurois natator

(Ranidae) (4.16%),

Limnonectes magnus

(Dicroglossidae) (2.08%),

Pulchrana grandocula

(Ranidae)(2.08%),

Philautus acutirostris

(Rhacophoridae) (2.08%),

Kalophrynus sinensis

(Microhylidae) (1.37%),

Philautus poecilius

(Rhacophoridae) (1.37%),

Limnonectes parvus

(Dicroglossidae) (0.69%),and

Platymantis

cf.

dorsalis

(Cetatobatrachidae)(0.69%).

Figure 4 Characteristic appearance of Type II microhabitat.

Figure 5 Characteristic appearance of Type III microhabitat.

In the lower montane forest (1000-1400 masl),eight species belonging to five families were documented,namely:Bufonidae,Megophyridae,Microhylidae,Ranidae,and Rhacophoridae.Still,the Mindanao Faunal Region endemic species

Ansonia muelleri

was the most abundant species recorded with 78.30%relative abundance followed by

Limnonectes magnus

(9.43%),

Staurois natator

(3.77%),

Megophrys stejnegeri

(3.77%),

Rhacophorus.bimaculatus

(2.83%),

Pulchrana grandocula

(0.94%),and

Philautus poecilius

(0.94%).

3.2. Species Accounts

Bufonidae

(Boulenger,1887)

Ansonia muelleri

(Figure 7) was documented from 1000-1600 masl and was observed in aquatic and terrestrial microhabitats.Specimens were collected and observed those exposed on forest ground,on top or among leaf litter on forest trails,and also on or beneath rocky crevices in mountain river systems or on stream banks.

A.muelleri

has been recorded on mountains in Mindanao such as Mt.Sinaka and Mt.Hamiguitan (Ates and Delima,2008),Mt.Malindang (Nuñeza

et al

.,2010),Mt.Pasian(Siler

et al

.,2009) and across Mindanao island (Sanguila

et al

.,2016).This species is widely distributed in the Mindanao Faunal Region.

Ansonia muelleri

had SVL ranging from 22-30 mm;HL=9-12 mm;HW=8-4 mm;tympanum width (TW)=7-8 mm;eye diameter (ED)=2-4 mm;forelimb length (FL)=17-23 mm;hind limb length (HiL)=23-40 mm;body weight (BW)=1-4 g.

A.muelleri

has a variable color pattern.However,most of the observed

A.muelleri

had alternate dark brown,green,and black straight lines running from the snout to vent;prominent dark bands on its forelimbs and hind limbs;and toes are webbed except for the 4th toe,which has the distal portion free of webbing.

Ceratobatrachidae

cf.(Duméril,1853)

Figure 6 Characteristic appearance of type IV microhabitat.

Figure 7 Ansonia muelleri (Least Concern;NSM4001),a Mindanao Faunal Region endemic,abundant in terrestrial and aquatic microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Platymantis

cf.

dorsalis

(Figure 8)was found inhabiting terrestrial microhabitat from 1400-1600 masl,specifically in the leaf litter along the riparian system.This species is a Philippine endemic.The captured

Platymantis

cf.

dorsalis

had the following measurements:SVL=1.6 mm;HL=2.4 mm;HW=0.7 mm;TW=0.8 mm;FL=1.1 mm;HiL=2.4 mm;ED=0.2 mm;BW=3 g.This recorded species had a prominent golden-yellow color from snout to the middle of the orbit.It also had numerous dark crossbars on dorsal surfaces of its hindlimbs and forelimbs.

Dicroglossidae

(Stejneger,1910)

Limnonectes magnus

(Figure 9) was recorded in both aquatic andterrestrial microhabitats at 1000 -1600 masl on Mt.Kalo-Kalo.Specimens were observed sitting on rocks,boulders of mountain streams,or hidden among leaf litter on the forest ground near stream banks.This species has a wide distribution and is endemicto the Mindanao Faunal Region.

Figure 8 Platymantis cf.dorsalis (Least Concern;NSM4002),a Philippine endemic,abundant in terrestrial microhabitats(1400-1600 masl).Photo by V.C.P.DELA TORRE.

Figure 9 Limnonectes magnus (Near-Threatened;NSM4003),a Mindanao Faunal Region endemic,abundant in aquatic and terrestrial microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Limnonectes magnus

had the following measurements:SVL=57.5-73 mm;HL= 27.5-33 mm;HW=22--3 mm;TW=23.5-29;FL=31-52 mm;HiL=94-105;ED=7.5-10 mm;BW=20-60 g.Specimens encountered had a visible tympanum;and dark bands on forelimbs and hind limbs.Laterally,they had light yellow spot near the groin;tympanic fold was present from snout to base of forelimbs;dorsal body granular to tuberculate skin;and the ventral body had smooth skin.

(Taylor,1920)

Limnonectes parvus

(Figure 10) was recorded inhabiting terrestrial microhabitats at 1400-1600 masl.This species can be commonly encountered in central,southern,western,and northeastern Mindanao (Sanguila

et al

.,2016).This species is endemicto the Mindanao Faunal Region.The captured

Limnonectes parvus

had the following measurements:SVL=3.5 mm;HL=1.5 mm;HW=6 mm;TW=1.2 mm;FL=2.8 mm;HiL=1.5 mm;ED=3 mm;BW=3 g.This species had a prominent golden-yellow color from its snout to vent.Also numerous dark crossbars in its hindlimbs and forelimbs can be observed.

Megophryidae

(Brown,Siler,Diesmos and Alcala,2009)

Leptobrachium lumadorum

(Figure 11) is widely distributed throughout the upper montane forest of Mt.Kalo-Kalo inhabiting riparian habitats.Moreover,this species was recorded as widespread on Mindanao and Basilan islands,but not present on Dinagat,Siargao,Leyte,Samar,and Bohol(Brown

et al

.,2009). This species is endemic to the Mindanao Faunal Region.

Leptobrachium lumadorum

had the following measurements:SVL=4.2-4.5 mm;HL=2.1-2.3 mm;HW=1.9-2.1 mm;TW=2.0-2.2 mm;ED=0.7-0.9 mm;FL=2.8-3.2 mm;HiL=5.3-5.6 mm;BW=5-6 g.The

L.lumadorum

encountered had alternating brown bands on the forelimbs and hindlimbs,a visible tympanum,and a spotted-brown pattern on its dorsum.

(Taylor,1920)

Megophrys stejnegeri

(Figure 12) was observed in the lower montane forest from 1000-1400 masl on Mt.Kalo-Kalo.It uses terrestrial and aquatic microhabitats as well as on standing water pools.This species is considered widespread and endemic to the montane regions of the Mindanao Faunal Region like Mt.Sinaka,Mt.Hamiguitan (Ates and Delima,2008),Mt.Pasian(Siler

et al

.,2009),Mt.Malindang (Nuñeza

et al

.,2010),Samar,Leyte,Bohol,and Siargao Island (Diesmos

et al

.,2014;Diesmos

et al

.,2015).

Figure 10 Limnonectes parvus (Least Concern;NSM4004),a Mindanao Faunal Region endemic,abundant in terrestrial microhabitats (1400-1600 masl).Photo by V.C.P.DELA TORRE.

Figure 11 Leptobrachium lumadorum (Least Concern;NSM4005),a Mindanao Faunal Region endemic,utilizes aquatic and terrestrial microhabitats (1400-1600 masl).Photo by V.C.P.DELA TORRE.

Figure 12 Megophrys stejnegeri (Least Concern;NSM4006),a Mindanao Faunal Region endemic,utilizes aquatic and terrestrial microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Megophrys stejnegeri

had the following measurements:SVL=41 mm;HL=13 mm;HW=13.5 mm;TW=12.5 mm;FL=21 mm;HiL=67 mm;ED=5.5 mm;BW=10 g. This specimen had an observable brownish-orange color;a pair of longitudinal folds on the back;dark bands on forelimbs and hind limbs present;visible tympanum,and a horn-like projection over each eyelid.

(Peters,1867)

A juvenile of

Kalophrynus sinensis

(Figure 13) was captured in the upper montane forest at 1400-1600 masl.It occupies terrestrial and aquatic microhabitats.It is considered a widespread species,having been recorded from Basilan,Bohol,Camiguin Sur,Culion,Dinagat,Leyte,Mindanao,and Samar islands (Diesmos

et al

.,2015).

Kalophrynus sinensis

is frequently encountered in the rainy season,calling while floating on temporary pools or water-filled cavities in a variety of habitats of varying levels of disturbance.This species is endemic to the Mindanao Faunal Region.The juvenile

Kalophr ynus sinensis

had the following measurements:SVL=15 mm;HL= 7 mm;HW=6 mm;TW=6 mm;FL=10 mm;HiL=8 mm;ED=3 mm;BW=0.5 g.This species had a brown-orange color,usually with dark spots anteriorly and a dark triangle in the upper part of the head.The lower surfaces were dirty white with numerous black spots and the hindlimbs had dark crossbars.

Ranidae

(Taylor,1920)

Figure 13 Kalophrynus sinensis (Least Concern;NSM4007),a Mindanao Faunal Region endemic,utilizes aquatic and terrestrial microhabitats (1400-1600 masl).Photo by V.C.P.DELA TORRE.

Pulcharana grandocula

(Figure 14) is commonly encountered at high abundances and distributed throughout the Mindanao PAIC islands (Brown and Siler,2013).This species can be found in a variety of disturbed habitats and is distributed across much of the elevational relief of Mindanao (Sanguila

et al

.,2016).In this study it was recorded in the lower and upper montane forests at 1000-1600 masl,inhabiting the aquatic and terrestrial microhabitats.The discovery of a new,morphologically similar,and exceedingly rare stream frog species that had previously been confused with

Hylarana grandocula

(Brown and Siler,2013;Brown,2015) led Brown and Siler (2013) and Brown(2015) to speculate that mountains of northeast Mindanao may also harbor undocumented populations of this second Mindanao

Hylarana

taxon.Oliver

et al

.(2015) recently published a phylogeny for many members of the African,Papuan,and Southeast Asian members of the genus

Hylarana

and recognized“

Pulchrana

”as the available name corresponding to the

Hylarana signata

complex (Brown and Siler,2013).Although this action is arbitrary and unnecessary and no justification for a maximally reduced classification was provided (Wiens

et al

.,2009;Poe,2013;Brown,2015),the most recently published name was adopted.

Pulchrana grandocula

had the following measurements: SVL=54 mm;HL=29 mm;HW=22 mm;TW=18 mm;FL=41mm;HiL=121 mm;ED=8 mm;BW=15 g.This species had a brown-orange color,usually with dark spots anteriorly and a brown margin on the side of its dorsal body.Hindlimbs and forelimbs had prominent dark bands.

(Günther,1858)

Staurois natator

(Figure 15) was observed to be widely distributed in the lower and upper montane forests at 1000-1600 masl.Mainly inhabiting the terrestrial and arboreal microhabitats,this species was commonly found on leaf axils of ferns and Pandaceae.Common throughout the Mindanao Faunal Region,

Staurois natator

is a frequently observed component of most amphibian communities of the southern Philippines (Alcala and Brown,1998).Arifin

et al

.(2011) demonstrated the distinction between Palawan faunal region populations (

S.nubilis

) versus those of the Mindanao PAIC (

S.natator

).

Figure 14 Pulchrana grandocula (Least Concern;NSM4008),a Mindanao Faunal Region endemic,utilizes aquatic and terrestrial microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Table 1 Species composition,relative frequency (),distribution,and conservation status of anurans on Mt.Kalo-Kalo,Mt.Kalatungan Range Natural Park,Philippines.

Staurois natator

had the following measurements:SVL of 25-28.5 mm;HL=11-13 mm;HW=8-8.5 mm;TW=12-13.5 mm;FL=14-16 mm;HiL=59-62 mm;ED=4-4.5 mm;BW=1.5-2 g.The species observed had a uniformly brownish dorsal skin color,usually with green spots anteriorly and a green venter.Hind limbs and forelimbs had brown bands.

Rhacophoridae

(Peters,1867)

Philautus acutirostris

(Figure 16) was recorded in the upper montane forest at 1400 -1600 masl on Mt.Kalo-Kalo inhabiting arboreal microhabitats.This small shrub frog is known to be widely distributed on Jolo and Basilan islands of the Sulu Archipelago,Zamboanga del Sur Province of western Mindanao,and on the mountains of the northeast Mindanao(Brown and Alcala,1994;Sanguila

et al

.,2016).This species is endemic to the Mindanao Faunal Region.

Philautus acutirostris

had the following measurements: SVL=0.5-0.6 mm;HL=0.7-0.9 mm;HW=0.5-0.6 mm;TW=0.6-0.8 mm;FL=1.0-1.1 mm;HiL=2.2-2.4 mm;ED=0.1-0.2 mm;BW=3 g.The species observed had a uniformly brownish dorsal skin color,usually with brown spots anteriorly and brown venter,and black lateral line from snout to vent.It had prominent lateral folds from its eyes down to its forelimbs.Hind limbs and forelimbs had black bands.

(Brown and Alcala,1994)

Figure 15 Staurois natator (Least Concern;NSM4009),a Mindanao Faunal Region endemic,abundant in arboreal and terrestrial microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Figure 16 Philautus acutirostris (Least Concern;NSM4010),a Mindanao Faunal Region endemic,abundant in arboreal microhabitats (1400-1600 masl).Photo by V.C.P.DELA TORRE.

This Mindanao Faunal Region endemic shrub frog was recorded in the lower and upper montane (1000-1600 masl)forests of Mt.Kalo-Kalo inhabiting arboreal microhabitats.

Philautus poecilius

(Figure 17) was also widely observed from the forests of eastern Mindanao (Brown and Alcala,1994;Plaza and Sanguila,2015) up to the high elevation forests of Mt.Lumot(Sanguila

et al

.,2016) and Mt.Malindang of western Mindanao(Nuñeza

et al

.,2010).

Philautus poecilius

had the following measurements:SVL=1.5-1.8 mm;HL=0.7-0.8 mm;HW=0.5-0.6 mm;TW=0.6-0.7 mm;FL=1.2-1.4 mm;HiL=1.1-1.2 mm;ED=0.2-0.3 mm;BW=0.5 g.The species observed had a uniformly spotted brown and black dorsal skin color,usually with brown spots anteriorly and brown venter.Hind limbs and forelimbs had black bands.

(Peters,1867)

Figure 17 Philautus poecilius (Least Concern;NSM4011),a Mindanao Faunal Region endemic,abundant in arboreal microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Figure 18 Rhacophorus bimaculatus (Least Concern;NSM4012),widespread in Luzon and Mindanao Faunal Region utilizes arboreal microhabitats (1000-1600 masl).Photo by V.C.P.DELA TORRE.

Rhacophorus bimaculatus

(Figure 18) utilizes arboreal microhabitats.It was observed in the lower and upper montane forests of Mt.Kalo-Kalo at 1000-1600 masl on the leaf axil of ferns.This species is known to be widespread in the Luzon and Mindanao Faunal Regions.This common tree frog inhabits overhanging understory vegetation surrounding rapidly cascading streams in lower to mid-montane forests.Its distinctive advertisement call is a single brief,high frequency,shrill chirp and can be heard over the sound of waterfalls(Sanguila

et al

.,2016).Previously considered uncommon,this species is now appreciated for its very specific microhabitat preference,where it can be predictably encountered by experienced field workers.Originally classified as“Near-Threatened”in 2010 (NT;IUCN 2010),and“Vulnerable”in 2016 (VU;IUCN 2016);this species now qualifies only for“Least Concern”status (LC;IUCN,2018) as a result of the numerous new localities at which it has been recorded (Gonzales

et al

.,2014),and the predictability where it can be found now that its habitat is known and can be purposefully surveyed (Diesmos

et al

.,2014,2015).

Rhacophorus bimaculatus

had the following measurements:SVL=30-32 mm;HL=13 -14 mm;HW=13.5-14 mm;TW=12.5-13 mm;FL=22.5-23 mm;HiL=59-60 mm;ED=4.5-5.5 mm;BW=3-4 g.This observed species had a highly variable color pattern,usually with grey spots anteriorly and yellow green venter.Hind limbs and forelimbs had brown bands.

3.3. Biodiversity Indices

Table 2 shows the biodiversity indices of the two sampling sites on Mt.Kalatungan.Our results indicate very low species diversity following the modified biodiversity scale of Fernando

et al

.(2004) in the upper montane (H’=1.276) and in the lower montane (H’=0.851)forests with uneven distribution.

3.4. Microhabitats of Anurans

Gonzales and Dans (1994)defined four microhabitat types,although we have further classified these into five specific microhabitats such as bodies of water,rocks along streams/rivers,shrubs growing near the stream,shrubs growing in the forest,and fallen logs.The majority of the species recorded can be both aquatic and terrestrial that are found within or near bodies of water(Table 3).Most anurans were observed on rocks along streams and rivers,on shrubs growing in the forest,and on fallen logs.

Staurois natator

was also found inhabiting the leaf axils of ferns and different shrubs near the stream.Three species,

Philautus acutirostris,Philautus poecilius,

and

Rhacophorus bimaculatus

were strictly found in arboreal microhabitats (forest shrubs),whereas

Limnonectes magnus

and

Ansonia muelleri

were observed to have overlapping microhabitats.

4.Discussion

The presence of endemic anuran species,including ten Mindanao Faunal Region endemics and two Philippine endemic anurans,in this study suggests that Mt.Kalo-Kalo of the Mt.Kalatungan Range Natural Park (MKaRNP) is an area of local conservation value in which suitable habitats still exist to support endemic anuran communities.Only

Limnonectes magnus

is“Near-Threatened”whereas the rest of the taxa are categorized as“Least Concern”according to IUCN (2018).Despite being listed as“Near-Threatened”

,

Limnonectes magnus

was the second most abundant species in the study area.Its ability to inhabit undisturbed and disturbed streams and rivers in lower montane and lowland forests explains its abundance(IUCN SSC Amphibian Specialist Group,2019).Recently conducted herpetofaunal surveys by local herpetologists in the Philippines listed

Ansonia muelleri

as“Vulnerable”(Philippine Red List Status,2019). In this study,

Ansonia muelleri

was the most abundant species.The depressed body,strong tail,reduced tailfins,and sucker-like mouth of the tadpole of

Ansonia muelleri

suits this species for rapidly-running streams (Boulenger,1912;Taylor,1922;Inger,2007) found in the study area.More anuran species were recorded in the upper montane forest (1400-1600 masl) than in the lower montane forest(1000-1400 masl).Moreover,results also showed higher anuran diversity in the upper montane compared to the lower montane forest.Similar findings were reported by Warguez

et al

.(2013) and Toledo-Bruno

et al

.(2017) on MKaRNP,in which herpetofaunal species diversity was slightly higher at 1200-1600 masl.Several faunal surveys throughout the Philippines showed decreasing diversity with increasing elevations (Heaney and Rickart,1990;Diesmos

et al

.,2002;Nuneza

et al

.,2010;Siler

et al

.,2006).However,no trend was established in this study because there were only two sites sampled.Although the highest peak of MKaRNP is around 2880 masl,the peak at the sites we sampled within the mountain range on Mt.Kalo-Kalo was lower at 1730 masl.However,due to difficult accessibility and safety issues we did not conduct sampling at higher elevation or at the peak.Previous ecological studies of anuran species richness at different elevations in certain Long-Term Ecological Research(LTER) sites on Mindanao mountains also showed higher anuran species richness at high elevation.For instance,Mt.Malindang at 1600-1700 masl has the highest anuran species richness (

n

=11) of the four LTER sites (Mohagan

et al

.,2018).The species richness in this study is higher compared to anuran species richness on Mt.Hamiguitan with 10 species at 1400-1700 masl.However,Mt.Malindang has higher total species richness (

n

=20) considering various vegetation types from elevation of 900 to 1700 masl (Nuneza

et al

.,2010).Mt.Matutum also has higher species richness (

n

=13) at 500-1719 masl(Nuneza

et al

.,2017),but the montane forest has lower species richness (

n

=10) compared to the present study.Moreover,Mt.Kalo-Kalo’s 12 species is lower compared to Mt.Hamiguitan(

n

=15) at 545-1435 masl (Delima

et al

.,2007) and Mt.Hilong-Hilong (

n

=27) at 700-1300 masl (Plaza and Sanguila,2015).Compared to the four LTER sites of Mohagan

et al

.(2018) on Mt.Apo (

n

=5) at 1900-2000 masl,Mt.Hamiguitan (

n

=10) at 1000-1100 masl,Mt.Malindang (

n

=11) at 1600-1700 masl,and Mt.Kitanglad (

n

=6) at 2100-2200 masl,Mt.Kalo-Kalo of the MKaRNP has the highest species richness (

n

=12).In addition,all of these Mindanao mountains have high anuran endemism.For instance,the four LTER sites of Mohagan

et al

.(2018) on Mt.Apo and Mt.Kitanglad has 100% endemism,90% endemism on Mt.Hamiguitan,and 90% endemism on Mt.Malindang.Moreover,Mt.Hilong-Hilong has 100% endemism (Plaza and Sanguila,2015) and 90% endemism on Mt.Matutum (Nuneza

et al

.,2017).

Table 2 Anuran biodiversity indices in the lower and upper montane forests of Mt.Kalo-Kalo,Mt.Kalatungan Range Natural Park,Bukidnon.

Table 3 Microhabitats and relative frequency () of anurans on Mt.Kalo-Kalo,Mt.Kalatungan Range Natural Park,Bukidnon,Philippines.Legend:[]Plant species;＊Mindanao faunal region endemic;＊＊Philippine endemic.

Generally,species richness of anurans is highest at lower elevations especially those anurans requiring water bodies for reproduction such as streams and rivers.However,in the case of anurans that are direct developers,diversity increases with increasing elevation particularly in the montane forest(Diesmos

et al

.,2005;Fu

et al.

,2006;Mohagan

et al

.,2018).Some frogs in the families Ceratobtrachidae and Rhacophoridae are known to exhibit a terrestrial development type of reproductive mode,and are thus capable of undergoing direct development(Alcala,1962;Alcala and Brown,1982).In this study,33% of the total number of endemic species belong to these families.This may be related to amphibian ecological and physiological tolerances and microhabitat preferences.The upper montane forest itself has a patchy,range-restricted distribution to higher elevation in the topographically complex Mindanao Faunal Region (Diesmos and Brown,2011;Mohagan

et al

.,2018).The study on Mt.Kalatungan Range Natural Park(MKaRNP) conducted by Warguez

et al.

(2013) in Sitio San Guinto,Barangay Bacusanon,Municipality of Pangantucan,Bukidnon Province (7.90658°N;124.72382°E;7.92474°N;124.73241°E) at 1208-1600 masl.,recorded 14 species of anurans but Toledo-Bruno

et al

.(2017) in Barangay Portulin,Municipality of Pangantucan,Bukidnon Province (4°22’33.36”N,128°21’58.70”E) at 1200-1600 masl,recorded only half this number from May-June 2016,five years later (Table 4). Species earlier reported but not observed in our study include

Ansonia mcgregori

,

Pelophryne brevipes,Limnonectes

cf.

ferneri,Fejervarya moodiei,Occidozyga laevis,Philautus surrufus,

Philautus worcesteri

,and

Polypedates leucomystax

.Seasonal variation and atmospheric variation (precipitation) may also explain some differences in species recorded previously and in the present study on Mt.Kalatungan.Despite not having observed some previously recorded species from another area on Mt.Kalatungan Range Natural Park,we encountered three species that were not documented in earlier studies.These species are

Limnoectes parvus,

Leptobrachium lumadorum,

and

Philautus

cf.

dorsalis

which inhabit both the lower and upper montane forests at 1000-1600 masl.These species have very low abundance in the study area,which probably explains why Warguez e

t al

.(2013) and Toledo-Bruno

et al

.(2017) failed to document them in their studies.Other species like

Megophrys stejnegeri

,

Kalophrynus sinensis

,

Pulchrana grandocula,Staurois natator

,and

Philautus poecilius

have low abundance and were not documented by Toledo-Bruno

et al

.(2017).Overall,seven families were observed on MKaRNP,namely:Bufonidae (

Ansonia mcgregori,A.muelleri,

Polyphryne brevipes

),Ceratobatrachidae (

Philautus

cf.

dorsalis

) Dicroglossidae(

Limnonectes

cf.

ferneri,Limnonectes parvus,

Limnonectes magnus

),Megophryidae (

Megophrys stejnegeri,Leptobrachium lumadorum

),Microhylidae

(Kalophrynus sinensis

);Ranidae (

Fejervarya moodiei,Occidozyga laevis,Pulchrana grandocula,Staurois natator

),and Rhacophoridae (

Philautus acutirostris,Philautus poecilius,Philautus surrufus,Philautus worcesteri,Polypedates leucomystax,Rhacophorus bimaculatus

).With the previous studies and the present results,MKaRNP has now a total of 20 species of anurans.Despite the protected status of Mt.Kalatungan Range Natural Park (MKaRNP),anthropogenic activities such as unregulated harvesting of frogs (

Limnonectes magnus

),slash and burn farming,conversion of some areas in the lower and upper montane forests to farmland,and improper disposal of garbage pose considerable threats to the anuran population of the mountain range.Since most of the endemic anurans on Mt.Kalo-Kalo of MKaRNP were found on rocks along streams,rivers,fallen logs,and leaf litter microhabitat,threats like deforestation and habitat destruction may affect anuran assemblages (Lehtinen

et al

.,1999).Results suggest that despite the anthropogenic disturbances,the lower and upper montane forests of Mt.Kalatungan Range Natural Park remain suitable habitats for endemic anurans.

Acknowledgments

We would like to acknowledge the OVCRE-MSU-IIT and DOST-ASTHRDP-NSC for the funding support and Department of Environment and Natural Resources—Northern Mindanao (Region X) for the issuanceof the Gratuitous Permit.We would like also to extend our gratitude to Dr.Rafe M.BROWN for validating the anuran species identification and Dr. Christine F.GODINEZ-ORTEGA for editing the manuscript.

Table 4 Anuran species of Mt.Kalatungan Range Natural Park.Legend:＊Mindanao Faunal Region endemic;＊＊ Philippine endemic.