IJBPAS, July, 2018, 7(7): 1362-1373 ISSN: 2277–4998

MINALUNGAO NATIONAL PARK, , HOSTS SIX CHIROPTERA SPECIES

KHRISTINA G. JUDAN CRUZ AND LORD MER DG. PADER Department of Biological Sciences, State University, Science City of Munoz, Nueva Ecija, Phil- ippines *Corresponding author: Khristina G. Judan Cruz: E-mail: [email protected] Received 26th Feb. 2018; Revised 30th March. 2018; Accepted 22nd April 2018; Available online 1st July 2018

https://doi.org/10.31032/IJBPAS/2018/7.7.4491 ABSTRACT Order Chiroptera is the most diverse mammalian order in the Philippines. However, the Chiropterans are also likely the most poorly identified in the Philippines. Spe- cies of Chiroptera were collected from three (3) caves at , a 2000- hectare protected area located at , Nueva Ecija in Central Luzon, Philippines, which has not yet been identified for research, hence, limited existing published scientific studies. This is the first report of Chiropterans on Minalungao National Park, Philippines based on morphological characters, an update on the previously reported species based on a molecular marker, the mitochondrial cytochrome oxidase I (mtCOI). One endemic species is reported. The study revealed a high diversity of chiropteran species at Minalungao. A total of 6 species of Chiroptera representing 2 suborders (Megachiroptera and Microchiroptera) and 5 families (Vespertilionidae, Hipposideridae, Emballonuridae, Pteropodidae, and Rhinolophi- dae) were identified using morphological characterization. These are: Miniopterus australis (Kulilit), Hipposideros pygmaeus (Tengang Baboy), Taphozous melanopogon (Ngusong Ka- bayo), Rhinolophus arcuatus (Panget), jagori (Bangaag) and amplex- icaudus (Bayakan).

Keywords: Chiroptera; Minalungao National Park

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INTRODUCTION need for conservation movements is Although known for its small land caused by the devastation and damage of area, the Philippine archipelago is notable tropical forests and other anthropogenic for the huge number of native endemic threats such as hunting [1, 11]. mammalian species and has the highest Forest habitats have been acknowl- concentration of endemic mammals in a edged as principally essential for Chiropte- global scale with around 180 recorded ra and a priority for conservation efforts species; 110 of which are endem- globally [10] and the Philippines epito- ic [1, 2, 3, 4, 5, 6, 7). mizes an outstanding, if dismal, case. The Chiroptera species frequently fill forfeiture of forest habitats related to pre- up a high percentage of the diversity of all valent biodiversity have been well re- the mammals around the world [8]. Chi- ported [6, 11], although, this in combina- roptera is regarded as the most diverse or- tion with the comparatively high endem- der of mammals in the Philippines, with 25 ism and a rate of species discovery which megachiropteran and 48 microchiropteran is amongst the greatest in the world [3] described species [6,8]. Roughly 40% of likens to an urgent necessity for conserva- these species are endemic [8]. However, tion action. Accounted now as a hotspot in the Chiropterans are also accounted prob- terms of biodiversity loss, conservation ably as the least identified order of mam- strategies are now being instigated in mals in the Philippines [1,9]. In fact, only many areas in the Philippines. Among 70 species of Chiroptera were reported these is the establishment of national parks from the Philippines when the latest to help protect and conserve biodiversity. checklist was prepared in 1992 [3, 9]. Minalungao National Park located Chiroptera plays a very substantial at General Tinio, Nueva Ecija in Central role in the biosphere as part of the density Luzon, Philippines, is a 2000-hectare pro- and complexity of ecosystems and food tected area which has not yet been the fo- webs therein. As part of biodiversity, it cus for research and scientific studies. Pre- consumes fruits of trees as their nutrition sently, it serves as an ecotourism destina- and provides food, as well, to consumers tion under the local government unit exhi- such as humans. Protection of forest habi- biting stunning rock formations, fascinat- tats must be prioritized worldwide for the ing river, and enchanting flora. It boasts safety of Chiropterans [1,10]. The dire high diversity of organisms that are con-

1363 IJBPAS, July, 2018, 7(7) Khristina G. Judan Cruz et al Research Article densed on species-rich forests and rivers Currently, an initial listing of chi- and is also considered as one of the last ropteran species at Minalungao National natural environments north of .. It is Park based on molecular identification us- an ecologically and biologically significant ing the mitochondrial gene marker cyto- area where populations of globally threat- chorome oxidase 1 (CO1) was reported ened or geographically restricted species [14]. This is a first report on the chiropte- and undiscovered endemic species are ex- rans of based on morphological identifica- pected to be found. It is a very good area tion. With this study, it provides informa- for research particularly in studies for sys- tion on establishing its biodiversity that tematics, biodiversity conservation, mi- may be used to employ conservation strat- crobiology, ecology, and plant egies and eventually for the protection of physiology and biotechnology. These stu- Chiroptera at Minalungao National Park. dies would be useful in the identification MATERIALS AND METHODS of plants and animal species that dwell in Collection of Samples the area, as well as in determining the rela- The different species of Chiroptera tionships and its ecological interactions. were collected from three (3) caves at Mi- While new species of Chiropterans nalungao National Park such as Maipit have recently been reported, it is guessed Cave, Minalungao Cave and Makatulang that there are numerous species that may Cave. Exact location was determined using now be endangered and maybe extinct are the Global Positioning System (GPS). still unknown [1, 9]. Since it has been con- Consequently, abiotic factors such as air firmed that the assessment of the number temperature and humidity were determined of species of Chiroptera in Philippines that using thermo-anemometer and sling psyc- are extinct or endangered is not conceiva- hrometer respectively. The guidelines on ble, faunal surveys are recommended in handling wild for research were practically all parts of the country [12]. strictly followed. Around 50% of the megachiropteran fauna Morphological Identification of Chirop- in the Philippines is vastly threatened as an tera outcome of extensive deforestation and The following morphological charac- hunting [8, 10, 13]. On the other hand, the ters were used in identifying the collected status of Microchiropteran fauna is poorly Chiroptera based on [9]: (1) Total length; known [1,2] although several of endemic (2) Body length; (3) Ear; (4) Tail; (5) species were already recognized. Hindfoot; (6) Forearm.

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RESULTS AND DISCUSSION brown fur longer over the shoulders and A total of 6 species of Chiroptera top of the head than elsewhere on the representing 2 suborders (Megachiroptera body. Its tragus is small and is rounded and Microchiroptera) and 5 families (Ves- and widest at the tip. The tip of its longest pertilionidae, Hipposideridae, Emballonu- digit on the wing folds back rather firmly ridae, Pteropodidae, and Rhinolophidae) against the adjacent part of the wing, were identified. Eight phenotypes with dif- hence the English common name[15]. ferent local names were initially separated. It nestles about 1000 m above sea However, through morphological external level in agricultural areas, subsequent de- measurements, 3 of those phenotypes were velopment, and principal forest, rarely classified under one species, Taphozous comprising montane forest. It is frequently melanopogon Temminck, 1841 (Black- the most copious species in caves in dis- bearded tomb ) with local names of tracted territories, with assessments habi- Ngusong kabayo (brown), Ngusong ka- tually in the thousands. It often perches bayo (black). Other species identified with with Miniopterus schreibersii [4, 16, 17, common and local names were Miniopte- 18, 19, 20]. The echolocation call of this rus australis Tommes, 1848 (Little Bent- species from Laguna Province was defined Winged Bat/ Kulilit), Hipposideros pyg- [21]. They are geographically prevalent maeus Waterhouse, 1843 (Philippine and common but reliant on caves [15]. pygmy roundleaf bat/ Ngusong Baboy), Family Hipposideridae Rhinolophus arcuatus Peters, 1871 (Ar- Hipposideros pygmaeus Waterhouse, cuate horseshoe bat/ no known local 1843 (Philippine pygmy roundleaf bat/ name), Ptenochirus jagori Peters, 1861 Ngusong Baboy) (Greater musky fruit bat/Bangaag) and It has total length of 64.5 mm, tail Rousettus amplexicaudus E. Geoffroy, of 39.4 mm, hind foot of 2 mm, ear of 5.8 1810 (Common rousette/ Bayakan). mm, and forearm of 35.2 mm. The tiniest

Family Vespertilionidae species of Hipposideros is in the Philip- Miniopterus australis Tommes, 1848 pines. The dorsal pelage has two colors, (Little Bent-Winged Bat/Kulilit) white or cream at the base and dark brown It has a total length of 87 mm; tail at the tips. The ventral pelage is medium of 11.3 mm; hind foot of 6.2 mm; ear of brown, darkest at the base. There are two 13.4 mm; forearm of 63.7 mm. Similar to sets of leaflets lateral to the anterior nose- all Miniopterus, this species has very dark leaf, the interior pair of which meet over-

1365 IJBPAS, July, 2018, 7(7) Khristina G. Judan Cruz et al Research Article head the mouth (at the foot of the noseleaf) tions with huge attics, effortlessly evident to form a incessant leaflet[22]. in hazy daylight [18, 19, 20, 24] . It is pre- This species is not well characte- valent in Asia and plentiful in the Philip- rized and identified. This species has been pines [23]. caught in caves close to lowland forest, Rousettus amplexicaudatus E. Geoffroy, secondary lowland forest, from sea level to 1810 (Common rousette/Bayakan) at least 200 m, over eroded limestone and It has a total length of 100 mm, tail soils[19, 20]. It is common but may be of 13.6 mm, ear of 13 mm, forearm of 63.7 harmfully obstructed by the ruining of mm, and hindfoot of 6.2 mm. It is a huge cave habitats. Lately there are increased fruit bat, but males are significantly bigger captures, hence increased information. than females. Back fur is dark brown or However, further field studies are critically grey, frequently having an ice-covered required [22]. look, and is somewhat little and thin. The

Family Emballonuridae muzzle is elongated and jagged, and the Taphozous melanopogon Temminck, ears are moderately long. The wing mem- 1841 (Black-bearded tomb bat/Ngusong branes are dark brown but almost translu- kabayo) cent over the bones, which give the look of It has a total length of 89 mm, tail white stripes. It has a claw on the primary of 29.3 mm, hind foot of 19.3 mm, ear of edge of the wing. It is passive when held 14.5 mm, and forearm of 63.5 mm. It has a and seldom bites[25]. light brown fur with huge eyes, mild nasal It is common in rural and housing area, and a low rounded tragus. It has a tail areas up to 500 m and rare in agricultural that is covered inside the tail membrane areas from 500 to 1600 m. Furthermore, it for the basal half but penetrates the mem- is rarely in forest. All known nesting sites brane and lies on topmost of the mem- are in caves. Mature males are fewer than brane for the posterior half. Mature males mature females. The species settles in have a spot of dark brown hair beneath the huge groups (up to 100,000 per cave) and jowl [23]. may have a harem type of reproducing It is widespread in urban regions, system. They fly up to 25 km per night to in areas with limestone caves, and in sea forage. They naturally consume overriped caves, at elevations at or below 150 m. It fruit, producing less impairment in orc- often settles in narrow areas of caves and hards than is usually thought of [12, 16, in churches, libraries, and other construc- 17, 18, 26, 27, 28a 28b, 29]. It is prevalent

1366 IJBPAS, July, 2018, 7(7) Khristina G. Judan Cruz et al Research Article in Indo-Australia. It is locally abundant, 12, 17, 20, 26, 27 , 28a, 28b, 32, 33, 34]. normally firm, but exposed to extreme Its population is big and commonly con- hunting at some cave habitats [30]. stant, extensive, and forbearing of serious- ly bothered habitat [31]. Ptenochirus jagori Peters, 1861 (Greater musky fruit bat/Bangaag) Family Rhinolophidae It has a total length of 117.6 mm, Rhinolophus arcuatus Peters, 1871 (Ar- tail of 16.9 mm, ear of 14.6 mm, forearm cuate horseshoe bat; no known local of 87.6 mm, and hindfoot of 12.1 mm. It is name) an objectively huge fruit bat with a wide- It is a medium to small Rhinolo- ranging, black head and stouty snout. Oral- phus, with total length of 61 mm, hind foot ly, four upper and two lower incisors are of 19.6 mm, ear of 39.2 mm, and forearm present. Adults have a shoulder ruff of fur, of 56.4 mm. The fur is generally moderate typically with a gland below the ruff that brown posteriorly, and somewhat lighter secretes a yellow greasy substance, which anteriorly. The noseleaf is almost as broad marks the ruff. A smell of cinnamon is a as the muzzle, and there are no additional common distinguishing characteristic, es- leaflets [35]. pecially on males. Males are somewhat It can be seen from sea level to bigger and darker than females[31]. 1950 m, in farmlands, second growth, and It is plentiful in primary forest, primary forest, frequently abundant in the widespread in secondary forest, frequently lowlands but rarely in montane and mossy seen in farmland and urban parks and do- forest. Perching spots are in caves, fis- mestic areas. It is seen from sea level to at sures, rocky ledges, and in deep trees. It is least 1950 m. Frequently, it is one of the more effortlessly caught in harp ploys than most populous in lowland forest, with in haze nets [4, 16, 17, 18, 19, 21, 28a, densities of 1 to over 3 per hectare. Mature 28b, 36, 37, 38]. The echolocation calls of males have full length about half the size specimens from Laguna Province, Luzon of those of mature females. It consumes were defined [21]. They are prevalent and greatly on figs and other fruits such as ba- locally common [35]. nana (Musa spp.). Perching spots have A total of 6 chiropterans were iden- been discovered in hollow trees and in nar- tified at Minalungao National Park, Phil- row caves in limestone and clay panels. ippines using morphological characters. Genomic records infer equally high levels This embodies nearly 9% of the Philippine of gene flow throughout the Philippines [9, bat community out of the 68 species re-

1367 IJBPAS, July, 2018, 7(7) Khristina G. Judan Cruz et al Research Article ported [39]. The Philippine bat fauna un- vorous diet of some of the species of Chi- veils remarkably great rate of endemism, roptera, they are likewise referred to as definitely among the utmost in the world several of the most essential seed disper- [40]. In fact, one species reported in this sors, crucial for the redevelopment of the study, Ptenochirus jagori, is endemic to forests and establishment of the fresh the Philippines [41]. This great level of bat spaces by plants [44]. The occurrence of diversity and endemism may be caused by the bat species in the caves they were col- optimum environmental conditions of the lected gives us an idea of the diet of the region. Chiroptera predominantly occupies chiropterans and the species of plants and jungles and rich areas such as rivers that animals surrounding the location. give an essential territory for bat fauna by Since only morphological mea- giving uninterrupted treasured resources. surements were employed in the identifi- Riparian habitats, shown by the Minalun- cation, more molecular studies on these gao area that comprises rivers, are signifi- species, aside from the initial molecular cant habitats for many species of Chiropte- barcoding studies done [14], are now un- ra because it provides food and water. Bat derway to accurately verify species as- searching activity ensues prominently in signment as 8 initial phenotypes were cha- this type of habitat [42]. Moreover, high racterized with three different phenotypes diversity of the chiropterans maybe caused were classified only under one species, T. by the occurrence of trees and insects in melanopogon. Morphological identifica- the area that chiefly constitutes their diet. tion may be unreliable and can be chal- Furthermore, this diversity of bats lenging and it is not always conceivable to in the area shows the quality of the envi- classify bats only by outward characters ronment. With its environmental signific- [45] as specific species may be very com- ance on diverse habitats, Chiroptera is a parable in form, hence species assignment good indicator of integrity of natural as well as phylogeny can only be fixed us- communities because of its number of re- ing up-to-date molecular methods [45]. source qualities such as nestling, irrigat- Through succeeding researches, it is hoped ing, and nourishing habitats presenting that this opens up the idea of discovering rapid population variations if supply more endemic and unrecorded chiropte- attribute is misplaced [43]. The signific- rans in the Philippines, particularly at Mi- ance of recording the existing species in nalungao National Park as well as design- the area is signified. Because of the frugi-

1368 IJBPAS, July, 2018, 7(7) Khristina G. Judan Cruz et al Research Article ing strategies for its conservation and completion of the research, this piece of management. work is dedicated to them. CONCLUSION REFERENCES A total of 6 species of Chiroptera [1] Turner, CS, Tamblyn A, Dray R, representing 2 suborders (Megachiroptera Maunder L, Raines PS. 2003. The and Microchiroptera) and 5 families (Ves- biodiversity of the Upper Imbang- pertilionidae, Hipposideridae, Emballonu- Caliban Watershed, North Negros ridae, Pteropodidae, and Rhinolophidae) Forest Reserve, Negros Occidental, were identified using morphological cha- Philippines Coral Cay Conservation. racters. These are: Miniopterus australis London. (Kulilit), Hipposideros pygmaeus (Ten- [2] Heaney LR. 1993. Biodiversity gang Baboy), Taphozous melanopogon patterns and the conservation of (Ngusong Kabayo), Rhinolophus arcuatus mammals in the Philippines. Asia Life (Panget), Ptenochirus jagori (Bangaag) Sciences. 2, 261-274. and Rousettus amplexicaudus (Bayakan). [3] Heaney LR, Balete DS and Dans One endemic species is reported. ATL. 1997. Terrestrial Mammals. In ACKNOWLEDGEMENT Philippine Red Data Book. Wildlife The authors would like to Conservation Society of the acknowledge the following: Dr. Sweepea Philippines, Bookmark Inc, Veluz of the National Museum of the Philippines. Philippines, Manila for the authentication [4] Esselstyn JA, Widmann P and Heaney of the specimens and for sharing her LR. 2004. The Mammals of Palawan technical expertise; Prof. Thaddeus Island, Philippines. Proceedings of the Carvajal of De La Salle University- Biological Society of Washington. Manila, Philippines; Department of 117(3):271–302. Environment and Natural Resources – [5] Heaney LR, Balete DS, Dolar ML, CENRO, City, Nueva Ecija, Alcala AC, Dans ATL, Gonzales PC, Philippines; the Department of Biological Ingle NR, Lepiten MV, Oliver WLR, Sciences, Central Luzon State University, Ong PS, Rickart EA, Tabaranza Jr BR Science City of Munoz, Nueva Ecija; and and Utzurrum RCB. 1998. A synopsis most of all, the people of Minalungao of the mammalian fauna of the National Park, General Tino, Nueva Ecija, Philippine Islands. Fieldiana: Philippines for their assistance for the Zoology, New Series. 88:1–61.

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