Balo et al. 2021, Biologica Nyssana 12(1) 12 (1) September 2021: 71-78 DOI: 10.5281/zenodo.5523045 Bats assemblages in Awasian Water Forest Reserve, Tandag City, Surigao del Sur, Philippines Original Article Allyka Eve G. Balo College of Teacher Education, Surigao del Sur State University-Main Campus, Rosario, Tandag City, Suri- gao del Sur, Philippines allykaevebalo@gmail.com Mark Lee O. Sabandal College of Teacher Education, Surigao del Sur State University-Main Campus, Rosario, Tandag City, Suri- gao del Sur, Philippines malesab017@gmail.com Johnny B. Maglasang College of Teacher Education, Surigao del Sur State University-Main Campus, Rosario, Tandag City, Suri- gao del Sur, Philippines johnnymaglasang12345@gmail.com Lovely Jean B. Cosmiano College of Teacher Education, Surigao del Sur State University-Main Campus, Rosario, Tandag City, Suri- gao del Sur, Philippines cosmianolovelyjean14@gmail.com Arturo G. Gracia Jr. College of Teacher Education, Surigao del Sur State University-Main Campus, Rosario, Tandag City, Suri- gao del Sur, and Department of Natural Sciences and Mathematics, College of Arts and Sciences, Surigao del Sur State University-Main Campus, Rosario, Tandag City, Surigao del Sur, Philippines artzgracia@gmail.com (corresponding author) Received: Mart 19, 2020 Revised: October 11, 2020 Accepted: June 23, 2021 Abstract: Bats are an integral part of the ecosystem that plays a vital role in its stability. However, their existence is being threatened by uncontrollable anthropogenic activities, and its basic ecological information, especially in Eastern Mindanao, is limited. Thus, the study was conducted to evaluate the assemblage of bats in one of the underexplored sites of Eastern Mindanao Biodiversity Corridor. Mist-netting for a total of 9 net nights was carried out to document the species. A total of 10 species was observed. Among these species, Cynopterus brachyotis had the highest relative abundance comprising 53% of the population. Species diversity was relatively higher in the secondary mixed-dipterocarp forest with a Shannon-Weiner Diversity Index (H’) of 1.41 compared to the primary dipterocarp forest (H’=1.19). The species Ptenochirus jagori and Rhinolophus subrufus were the only bats observed with aggregated population distribution pattern. Among the recorded species, six (60%) were assessed as endemic comprising 5 Philippine and 1 Mindanao Endemic, while Eonycteris robusta and Rhinolophus subrufus were the Near-threatened species recorded. Based on the results, Awasian Water Forest Reserve houses an array of bat species with a high percentage of endemicity. Key words: assessment, diversity, endemism, volant mammals Apstract: Zajednica slepih miševa u rezervatu Awasian Water Forest, Tandag, Surigao del Sur, Filipini Slepi miševi su integralni deo ekosistema koji igraju vitalnu ulogu u njegovoj stabilnosti. Ipak, njihovo postojanje je ugroženo nekontrolisanim antropogenim aktivnostima i osnovne ekološke infomacije o njima su ograničene, posebno u istočnom Minadau. Zbog toga, sprovedeno je istraživanje kako bi se procenio raspored slepih miševa na jednoj od neistraženih lokacija koridora biodiverziteta u istočnom Minadau. Kako bi se dokumentovale vrste, izvršeno je postavljanje mreže tokom ukupno 9 noći. Utvrđeno je ukupno 10 vrsta. Među njima, Cynopterus brachyotis imao je najveću relativnu učestalost sačinjavajući 53% populacije. Diverzitet vrsta bio je relativno veći u sekundarnoj mešovitoj dipterokarpnoj šumi sa Shannon-Weiner indeksom diverziteta (H) od 1,41 u poređenju sa primarnom dikterokarpnom šumom (H=1,19). Vrste Ptenochirus jagori i Rhinolophus subrufus su jedini slepi miševi čije su populacije bile grupisanog rasporeda distribucije. Među zabeleženim vrstama, šest (60%) procenjene su kao endemične od koji 5 pripadaju Filipinskim a 1 Mindanao endemitima, dok vrste Eonycteris robusta i Rhinolophus subrufus predstavljaju skoro ugrožene vrste. Na osnovu rezultata, rezervat Awasian Water Forest je stanište za spektar vrsta slepih miševa sa visokim procentom endemizma. Ključne reči: procena, diverzitet, endemizam, leteći sisari © 2021 Balo et al. This is an open-access article distributed under the terms of the Creative Commons At- tribution License, which permits unrestricted use, distribution, and build upon your work non-commercially under the same license as the original. 71 Introduction The clade Chiroptera includes two extant clades, Megachiroptera (Old World Fruit Bats) and Micro- chiroptera (echolocating bats). Bats are considered as an ecological indicator because they control pests, pollinate fruit trees, and regenerate forests (Kasso and Balakrishnan, 2013). In the Philippines, bats are deemed as one of the most diverse mammals with at least 80 total extant species comprised of 26 meg- achiropteran and 54 microchiropteran species (Sed- lock et al., 2020). Of these, approximately 40% are reported to be endemic. However, uncontrolled an- thropogenic activities, habitat destruction, and dis- turbances are among the threats that threaten these taxa (Quibod et al., 2019). The Philippines is previously known for its dense forest in the early 20th century, with a reported for- est cover of 95% of the total landmass. However, the continuous deforestation resulted in massive forest denudation, which is estimated to be around 80 to 90% (Butler, 2014). Bats are highly forest-depend- ent animals, and changes in their habitat could de- crease their population and lead to eventual extinc- tion (Mickleburgh et al., 2002). This report is further supported by Murphy and Romanuk (2014) that mammalian species diversity, abundance, and along its mean biomass tend to decrease with increasing human disturbance and continuous habitat loss. For these reasons, the Philippines has been identified as an important area for bat diversity that prioritizes conservation efforts globally (Tanalgo and Hughes, 2018). Awasian Water Forest Reserve is one of the wa- tersheds of Mt. Hilong-hilong, a biodiversity corri- dor that lies between the provinces of Agusan and Surigao in the North Eastern Mindanao. Although reported to exhibit rich flora and fauna, these claims are mainly based on scientific expeditions done on the western side of the mountain ecosystem (Agu- san); and only a few to none scientific data can be retrieved to represent the eastern side (Surigao). The availability of ecological data is considered vi- tal since it serve as a basis for setting conservation priorities and guidelines (Goodman and Benstead, 2005; Mallari, 2009). Thus, this study was conduct- ed to address the scarcity of scientific information on bat community in the underexplored area of Mt. Hilong-hilong; and provide pragmatic findings that can be utilized for a better understanding of bat as- semblage in the area. Materials and Methods Place and Duration of the Study The study was conducted in the Awasian Water Forest Reserve located at Barangay Awasian, Tandag City Surigao del Sur Philippines (Fig. 1). The site is geographically located at 9°04’28.9”N and 126°08’34.7”E. The site is one of the watersheds of Mt. Hilong-hilong, situated in the south-eastern part of the mountain ecosystem. The study was conducted from October 1 to 9, 2017, covering nine days of sampling. The site’s topography is generally plain, rolling, and gently sloping. The climatic condition in the area falls under the Philippines’ Type II climate condition, which is characterized by rainfall distributed throughout the year, with a negligible short dry season (PAGASA, 2011). Establishment of Sampling Stations and Habitat Assessment Two 1-km transect lines were established in the study site with an aerial distance from each other of 200 meters. The first transect was considered as Sta- tion 1 that cut-across the dipterocarp forest. It was situated at an elevation that extends from 50 to 150 meters above sea level (masl). The dominant plant species were mixtures of Shorea spp., Ficus spp., and cultivated fruit trees like Lansium domesticum, Durio zibithenus, and Artocarpus odoratissimus. The soil-litter was thin and dry. The area’s distance to the nearest water body (stream) was around 5 to 100 meters. During the sampling period, the tem- perature ranges from 24 to 30 °C, with a general weather condition of calm-night with a clear sky. The second transect was designated as Station 2, established along the secondary mixed-dipterocarp forest. It was situated at an elevation of 100 to 250 m a.s.l. with a slightly-closed to closed canopy cover. The station’s dominant plant species were Shorea spp. of the family Dipterocarpaceae and Ficus spp. of family Moraceae. Soil-litter was dry but thicker as compared with Station 1. The area’s distance to the nearest stream was around 700 m, and 10 to 100 m from the small spring and stagnant canals. The tem- 72 BIOLOGICA NYSSANA ● 12 (1) September 2021: 71-78 Balo et al. ● Bats assemblages in Awasian Water Forest Reserve, Tandag City, Surigao del Sur, Philippines Fig. 1. Location map of Mt. Hilong-hilong and spot map of the study site. (BirdLife International, 2020) 73 perature during the sampling period ranged from 20 to 24 °C, with a general weather condition of gloomy with intermittent rain. Data Collection and Identification Along these transects, 21 Mist-nets with a dimen- sion of 4.5 meters long and 12 meters wide with a mesh size of 33 mm were established to capture the bats. Checking of nets was performed from 6:00 PM to 5:00 AM with 30 minutes to 1-hour interval to monitor if there were entangled bats and avoid pos- sible mortality. Captured species were placed into a cloth bag to prevent further stress on the organism and were brought to the processing area for taxo- nomic examination. The morphological metrics, which include ear (e), forelimb (fl), hindfoot (hf), tail (t), total length (TL), total body length (TBL), and teeth formation, were noted. These morphological metrics served as the bases for the identification of bat species. The dichotomous key for Philippine bats by Ingle and Heaney (1992) was used for species identification and classification. After taking all the taxonomic in- formation, bats were fed with a sucrose solution and were released back to their captured habitat. How- ever, upon the release, markings for each individual were considered to avoid count duplication if recap- tured. On the other hand, dead bat individuals were prepared as voucher specimens and were preserved directly in a 10% formalin solution. Data Analysis The Shannon-Weiner Diversity Index (H’) was used as the primary index to represent bats’ diversity. Along with this, the Species Diversity Equitability (Hmax) or the highest possible diversity index that can be obtained based on the given data set was also determined to assess how close the H’ index to the theoretical value. Moreover, the Simpson Diversity Index (1-D) and Species Evenness (J’) were calcu- lated to assess the level of species dominance and how evenly distributed the community’s population. With an interpretation that if the obtained 1-D and J’ values are closer to the value of one, means more diverse, and if it is closer to zero, indicates the op- posite. The species rarefaction curve was generated to represent the estimated species richness of bats in the sampled area and assess the bat sampling ad- equacy. For determining the species distribution, the sta- tistical analysis – chi-square was used to evaluate if the bat species’ populations are either random or aggregated. The level of significance used was 0.05 percent. The distribution probability values that are greater than the level of significance was given a random remark. In contrast, those with below the significance value are considered to have an aggre- gated distribution pattern. All these analyses were done using the Biodiversity Professional Software 2.0 by Macleece (1997). All ecological and conser- vation assessments were based on the International Union Conservation for Nature (IUCN) Redlist of 2020. Results and discussion Species Richness and Diversity A total of 196 individuals of bats belonging to three families and nine genera representing ten species were recorded. The species richness is comparative- ly lower than the records in Loboc Watershed, Mt. Irid, Mt. Kanlaon, Mt. Malindang, Mt. Matutum, Mt. Palali, Polilo Islands, and Sikatuna Protected Landscape. The discrepancy of the number of spe- cies observed is attributed to the sample size. The aforementioned studies had a larger sample area that crossed a broader elevational gradient and various vegetation types. On the other note, the result is ob- served to have a higher richness as compared to the records in Bagumbayan, Bega Watershed, Lowland Forest of Upland Cavite, Mt. Apo, Mt. Kalatungan, Mt. Kitanglad, Mt. Natib, and Cagayan de Oro River. The findings even equate with the number of species observed in the Expansion Site of Mt. Hamiguitan in Davao Oriental and Clarin River in Misamis Oc- cidental - even though these studies also covered a more extensive sampling area with at least four sam- pling stations (Tab. 1). With this, it could entail that Awasian Water For- est Reserve houses more bats with respect to the ra- tio and proportion between the species observed and the sampled area. The findings could also imply that the area has better ecological support for bat assem- blage since it can hold various species that even sur- passes some of those major mountain ecosystems in the Philippines like Mt. Apo and Mt. Kalatungan. A condition that conforms with the findings of Moha- gan et al. (2015) that bat richness tends to be higher in a forest ecosystem with more evident ecological support. Not to mention that probable new species could be added to the list if the sampling effort was extended as the species rarefaction depicts (Fig. 2). However, the chance is narrowing down as the data saturation is gradually flattening. As for diversity measures, the Secondary Mixed- dipterocarp forest showed to have a consistently bet- ter result in all the calculated diversity analysis com- pared to the Dipterocarp forest (Fig. 3). This result is attributed to a more complex plant structure that results in broader food options for bats. It was noted that at the course of the study, the explicitly observed fruit trees in the Secondary Mixed-dipterocarp forest BIOLOGICA NYSSANA ● 12 (1) September 2021: 71-78 Balo et al. ● Bats assemblages in Awasian Water Forest Reserve, Tandag City, Surigao del Sur, Philippines 74 like L. domesticum, D. zibithenus, and A. odoratis- simus were fruiting, thus, possibly attracting more species and population of bats in the said habitat. Not to mention that the dominant bat-guild observed was fruit bats; hence, the likelihood for the species to congregate in the area is plausible. The observa- tion aligns with the report of Hodgkison and Balding (2004) and Shafie et al. (2011) that bat diversity in a particular area is highly influenced by food avail- ability. Meanwhile, the overall all bat diversity in the area was revealed to be moderate. Among the species, Cynopterus brachyotis and Ptenochirus jagori were the well-docu- mented bats, wherein the two species com- prised 53 and 25 percent of the population, respectively (Fig. 4). The result conforms with various studies conducted in the Phil- ippine forests (Tab. 1). According to Tan et al. (1998), C. brachyotis is widely dis- tributed in the Southeast Asian Region and is common in the Philippine forest. The species also has a wide range of habitat preferences, extending from primary forest to disturbed habitats. While the species P. jagori is a common Philippine endemic bat observed in the lowland forests (Sedlock et al., 2008; IUCN, 2020). Table 1. Summary table of some of the bat studies conducted in the Philippines Site Species Richness Endemism (%) Dominant Species Observed References Bagumbayan, Sultan Kudarat 8 38 Cynopterus brachyotis Tanalgo (2017) Bega Watershed, Agusan del Sur 8 50 Cynopterus brachyotis Monteclaro and Nuñeza (2015) Cagayan de Oro River, Misamis Oriental 8 25 Cynopterus brachyotis Lobite et al. (2013) Clarin River, Misamis Occidental 10 40 Ptenochirus jagori del Socorro et al. (2018) Loboc Watershed, Bohol 15 40 Cynopterus brachyotis Joe et al. (2012) Lowland Forest, Upland Cavite 6 67 * Lagat and Causaren (2018) Mt. Apo, North Cotabato 8 38 Cynopterus brachyotis Achondro et al. (2014) Mt. Hamiguitan, Davao Oriental 10 40 Cynopterus brachyotis Amoroso et al. (2019) Mt. Irid, Southern Sierra Madre 16 19 Cynopterus brachyotis Balete et al. (2013) Mt. Kalatungan, Bukidnon 6 50 Haplonycteris fischeri Mohagan et al. (2018) Mt. Kanlaon, Negros Occidental 23 35 Cynopterus brachyotis Deligero et al. (2015) Mt. Kitanglad, Bukidnon 4 75 Alionycteris paucidentata Mohagan et al. (2015) Mt. Malindang, Misamis Occidental 19 47 Cynopterus brachyotis Nuñeza et al. (2006) Mt. Matutum, Saranggani 15 47 Cynopterus brachyotis Nuñeza et al. (2015) Mt. Natib, Bataan Province 9 33 Cynopterus brachyotis Rickart et al. (2013) Mt. Palali, Caraballo Mountains 12 42 Otopteropus cartilagonodus Alviola et al. (2011) Polilo Islands, Calabarzon 25 24 * Alviola (2010) Sikatuna Protected Landscape, Bohol 11 44 Cynopterus brachyotis van Vegchel (2003) Fig. 2. Species rarefaction plot in Awasian Water Forest Reserve BIOLOGICA NYSSANA ● 12 (1) September 2021: 71-78 Balo et al. ● Bats assemblages in Awasian Water Forest Reserve, Tandag City, Surigao del Sur, Philippines Species Distribution Pattern Across Habitats, Endemicity, and Conservation Status Out of the ten bat populations, the population of P. jagori (fruit bat) and R. subrufus (insectivorous bat) were noted as aggregated (p<0.05). On the other hand, the rest of the bat populations were noted as randomly distributed (p>0.05) (Tab. 2). The results could suggest two major points: First, for the case of P. jagori and R. subrufus, necessary ecological sup- port like food source is only found in a particular area or habitat and hence, the reason why the popu- lations of the two bats tend to cluster. Secondly, as for those bat populations with random distribution, the ecological factors that support the population are sporadically distributed in the area; hence, its popu- lation is also randomly distributed. This observa- tion conforms with the report of de Jong and Ahlen (1991) and Kush et al. (2004) that food source and supply are essential indicators for bat’s regional dis- tribution, especially for insectivorous bats. Among the ten documented species, five bats are assessed as Philippine endemic, and one is noted as Mindanao endemic. The assessment leads to com- 75 Table 2. Distribution pattern of bat’s population across habitats Taxon Variance Mean Chi-sq df. Probability Remarks PTEROPODIDAE Cynopterus brachyotis 24.5 52.5 0.4667 1 0.501796 Random Eonycteris robusta** 4.5 1.5 3 1 0.079335 Random Haplonycteris fischeri** 0.5 2.5 0.2 1 0.659200 Random Harpyionycteris whiteheadi** 0.5 1.5 0.3333 1 0.571066 Random Macroglossus minimus 12.5 7.5 1.6667 1 0.193468 Random Ptenochirus jagori** 420.5 24.5 17.1633 1 0.000066 Aggregated Ptenochirus minor* 18 5 3.6 1 0.054660 Random RHINOLOPHIDAE Rhinolophus subrufus** 12.5 2.5 5 1 0.023993 Aggregated VESPERTILIONIDAE Miniopterus schreibersi 0.5 0.5 1 1 0.318676 Random Pipistrellus sp. 0.5 0.5 1 1 0.318676 Random Note: Names with a double asterisk (**) are Philippine endemic bat species. While Names with a single asterisk (*) are Mindanao endemic Fig. 3. Comparative bar graph of Shannon-Weiner diversity index (H’), Maximum diversity index value (Hmax), Species diversity equitability (H’/Hmax), and Simpson diversity index (1-D) BIOLOGICA NYSSANA ● 12 (1) September 2021: 71-78 Balo et al. ● Bats assemblages in Awasian Water Forest Reserve, Tandag City, Surigao del Sur, Philippines prehensive documentation of 60% (6/10) total bat endemicity in the area. This total endemism is ob- served to be relatively higher than the bat endemism reported in various Philippine forests (Tab. 1), with an endemism percentage difference that ranges from 10 to 41 percent. Thus, suggesting that the area is an ideal abode to various endemic species. Meanwhile, among the bats, two species (E. robusta and R. sub- rufus) are evaluated to be under the Near-threatened category based on the IUCN 2017 and 2020 assess- ments. Under this criterion, the species are consid- ered to have a decreasing population and are subject to a threatened status if pressures on its existence will be unaddressed. According to IUCN (2020), the primary threat that affects these species’ populations is habitat loss. An evident threat in the buffer zones of the watershed. Conclusions Awasian Water Forest Reserve harbors various spe- cies of bats with high species endemicity. The pres- ence of bat species with random distribution patterns is advantageous to the area, for it contributes to a wider dispersion of ecological services like polli- nation and seed dispersal. Near-threatened species’ presence suggests further conservation efforts con- sidering that threats, especially from anthropogenic pressures, are evident. Acknowledgment. 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