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Key words: Argao Watershed Reserve, Copsychus cebuensis, microclimate and microhabitat variables, point count survey method, spatial distribution Factors Affecting the Spatial Distribution of Black Shama Copsychus cebuensis Steere, 1890 in Argao Watershed Reserve 1 Forestry Department, Cebu Technological University, Argao, Cebu Campus, Philippines 2 College of Forestry and Natural Resources, University of the Philippines Los Baños, College, Laguna 4031 Philippines 3 Institute of Biological Sciences, College of Arts and Sciences and School of Environmental Science & Management (SESAM), University of the Philippines Los Baños, College, Laguna 4031 Philippines 4 School of Environmental Science and Management, University of the Philippines Los Baños, College, Laguna 4031 Philippines § School of Environmental Science and Management, University of the Philippines Los Baños, College, Laguna 4031 Philippines *Corresponding author: [email protected] Archiebald Baltazar B. Malaki *, Rex Victor O. Cruz 2 , Nathaniel C. Bantayan 2 , Diomedes A. Racelis 2 , Inocencio E. Buot, Jr. 3 , and Leonardo M. Florece 4 Point count method was used to determine the microclimate and microhabitat factors affecting the population density and distribution of Black Shamas (Copsychus cebuensis) in Argao watershed (AWR) – a key biodiversity area on the island of Cebu and a top priority for conservation initiatives. Estimated population densities of C. cebuensis were 52 and 53 individuals per hectare in mixed and natural forests. There were only three and four predictors at habitat and sampling site level have able to explain the behavior of the population density of C. cebuensis. Relative humidity and canopy cover have high positive significant correlations, while tree basal area has high negative correlation (at the habitat level). Elevation and canopy cover have positive significant correlation, while slope and shrub cover have negative significant correlation with C. cebuensis population density (sampling site level). The adjusted R 2 values were 0.345 and 0.212 (at landscape and sampling site). These suggest that about 34.5% of the variations of the population density of C. cebuensis have been accounted for by the former and only 21.2% by the later. Preservation and protection of remaining forest fragments within AWR is paramount especially the four sampling sites being sampled. Philippine Journal of Science 147 (1): 175-189, March 2018 ISSN 0031 - 7683 Date Received: 18 Mar 2014 INTRODUCTION The survival of many species of birds is relatively dependent on the fluctuating environmental variables such as microhabitat and microclimate (Rosli et al. 2012). However, these responses may vary with species physiological tolerance, and most especially to nestlings (Hayworth & Weathers 1984; Burton 1995; Thomas et al. 2001; Harrison et al. 2003; Huntley et al. 2006; Hitch & Leberg 2007; Devictor et al. 2008; Virkkala et al. 2008; Rosli et al. 2012). Studies have shown that, species that prefer forest interior as primary habitat may avoid edges due to changes in microclimate, vegetation structure, 175
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  • Key words: Argao Watershed Reserve, Copsychus cebuensis, microclimate and microhabitat variables, point count survey method, spatial distribution

    Factors Affecting the Spatial Distribution of Black Shama Copsychus cebuensis Steere, 1890

    in Argao Watershed Reserve

    1Forestry Department, Cebu Technological University, Argao, Cebu Campus, Philippines2College of Forestry and Natural Resources, University of the

    Philippines Los Baños, College, Laguna 4031 Philippines3Institute of Biological Sciences, College of Arts and Sciences and School of

    Environmental Science & Management (SESAM), University of the Philippines Los Baños, College, Laguna 4031 Philippines

    4School of Environmental Science and Management, University of the Philippines Los Baños, College, Laguna 4031 Philippines

    §School of Environmental Science and Management, University of the Philippines Los Baños, College, Laguna 4031 Philippines

    *Corresponding author: [email protected]

    Archiebald Baltazar B. Malaki1§*, Rex Victor O. Cruz2, Nathaniel C. Bantayan2, Diomedes A. Racelis2, Inocencio E. Buot, Jr.3, and Leonardo M. Florece4

    Point count method was used to determine the microclimate and microhabitat factors affecting the population density and distribution of Black Shamas (Copsychus cebuensis) in Argao watershed (AWR) – a key biodiversity area on the island of Cebu and a top priority for conservation initiatives. Estimated population densities of C. cebuensis were 52 and 53 individuals per hectare in mixed and natural forests. There were only three and four predictors at habitat and sampling site level have able to explain the behavior of the population density of C. cebuensis. Relative humidity and canopy cover have high positive significant correlations, while tree basal area has high negative correlation (at the habitat level). Elevation and canopy cover have positive significant correlation, while slope and shrub cover have negative significant correlation with C. cebuensis population density (sampling site level). The adjusted R2 values were 0.345 and 0.212 (at landscape and sampling site). These suggest that about 34.5% of the variations of the population density of C. cebuensis have been accounted for by the former and only 21.2% by the later. Preservation and protection of remaining forest fragments within AWR is paramount especially the four sampling sites being sampled.

    Philippine Journal of Science147 (1): 175-189, March 2018ISSN 0031 - 7683Date Received: 18 Mar 2014

    INTRODUCTIONThe survival of many species of birds is relatively dependent on the fluctuating environmental variables such as microhabitat and microclimate (Rosli et al. 2012). However, these responses may vary with species

    physiological tolerance, and most especially to nestlings (Hayworth & Weathers 1984; Burton 1995; Thomas et al. 2001; Harrison et al. 2003; Huntley et al. 2006; Hitch & Leberg 2007; Devictor et al. 2008; Virkkala et al. 2008; Rosli et al. 2012). Studies have shown that, species that prefer forest interior as primary habitat may avoid edges due to changes in microclimate, vegetation structure,

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  • or high density predators or blood parasites (Yahner & Scott 1988; Malcom 1994; Marini et al. 1995; Stephens et al. 2003).

    The Black Shama Copsychus cebuensis (Passeriformis: Muscicapidae) is endemic to Cebu Island in the central Philippines. Locally known as ‘siloy’, it is a sedentary species that feeds on insects normally black beetles (Kennedy et al. 2000). This species inhabits primary forest and the dense undergrowth of secondary habitats (e.g., along steep ravines), particularly along ridge-top and valley-bottoms with a high percentage of canopy cover (Kennedy et al. 2000; Birdlife International 2012). Previous studies have also reported the species in scrub and cut-over forests, plantations, and bamboo groves, although Jakosalem and co-authors (2005) report that the species prefers forest habitats and may only tolerate degraded habitats as there are very few remaining forest patches in Cebu. It breeds annually, in between the dry months of February up to the wet months of September (Dutson et al. 1993).

    This species qualifies as Endangered as it has a very small range and population, both of which are continuously declining (Collar et al. 1999; Birdlife International 2001 & 2012; IUCN 2012). Additionally, it suffers from severe fragmentation owing to extreme pressure on the few remaining, already highly degraded, tracts of forest in Cebu Island that still support subpopulations (Collar et al. 1999; Birdlife International 2012). Likewise, biodiversity in Argao watershed is pervasively threatened from degradation posed by human activities including settlement, land use conversion, shifting cultivation, illegal cutting of trees for house construction, firewood gathering, and habitat clearance for mining (Malaki & Buot 2011). Consequently, these disturbances may eventually affect the microclimate and microhabitat factors in the watershed area and ultimately the present subpopulations of Copsychus cebuensis (Gonzalez et al. 1999; Jakosalem et al. 2005).

    A number of insectivorous species of forest birds are adapted to changes in microclimate and microhabitat factors (Arriaga-Weiss et al. 2008). Varesteh and co-workers (2010) showed that the distribution of some understorey birds species are also correlated with canopy cover, number of trees, and ground cover as the consequence of forest edge and gaps. However, avifaunal species may respond to one or a combination of these changes in the landscapes as a result of various mechanisms of may be biological origin (Robinson et al. 1995). Studying bird occurrences, densities and/or populations may therefore give a distinct result because of environmental and habitat changes over the forest in a long time (Rosli et al. 2012).

    Moradi and co-authors (2009), in their study of insectivorous birds of Malaysia, revealed that arboreal foliage gleaning insectivores were positively correlated

    with ground cover, light intensity, shrub cover, and percent of shrub cover. Terrestrial insectivores that were sensitive to the forest edge could indicate the quality of forest interior habitat associated with high humidity, dense canopy cover, and deep litter depth. A study of upper storey birds in Malaysia showed that bird responds are significantly correlated with environmental variables associated with various distances from the forest edge (Rosli et al. 2012).

    In the Philippines, the effects of anthropogenic land use on the natural habitats at Subic Bay Forest Reserve have been studied, showing that forest bird species are positively correlated with vegetation variables such as canopy cover, tree density, height to inversion, and ground cover (Posa & Sodhi 2006). Results further revealed that majority of the bird contacts were sensitive to canopy loss and requires 60% canopy cover and higher in order to maintain a good environmental condition for the birds.

    Landmark studies on Cebu Black Shama – including those by Bourns & Worcester (1894; McGregor 1909-1910) – described the species as “very rare” on Cebu and as the rarest of the Philippine shamas, with a very low population (Hachisuka 1936). By the end of the 1960s, based on the results of a decade of sporadic fieldwork reported on a decade earlier (Rabor 1959), it was regarded as “the only survivor among the ten endemic birds on Cebu” and (once again) “very...rare” (Birdlife International 2001). The species was also known to survive in a considerable number of localities in Cebu Province but rather in small numbers (Magsalay 1993; Dans & Gonzalez verbally 1996). The single largest population appears to be that at Casili, Consolacion consisting of around 50 birds in about c.10 km2 of fragmented scrub forest and bamboo thicket (Dutson et al. 1993).

    The Cebu Biodiversity Conservation Project – FFI and Darwin Initiative did an island-wide survey on the province, which lead to the rediscovery of the species in Argao (Gonzalez et al. 1999). Black Shama was also captured in the extensive mist-netting of birds conducted in Alcoy in Mar 2000 by Marisol dG. Pedregosa. Recently, in 2003-2004, a study on population and habitat preferences of the Black Shama funded by Rufford Small Grants for Nature Conservation and Threatened species Program of Haribon Foundation Inc. showed that subpopulations of Black Shama are present in considerable number especially in Nug-as forest in Alcoy, Cebu and in Argao municipality (Jakosalem et al. 2005). There have been studies conducted recently on the threatened and endemic species on Argao watershed, particularly in Mt. Lantoy Forest. Such studies had recorded the following species: Black Shama, Streak-Breasted Bulbul (Ixos siquijorensis monticola; Endangered), Everett’s White-eye (Zosterops everetti everetti), Black-Chinned Fruit Dove (Ptilinopus

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  • occipitalis), Variable Kingfisher (Ceyx lepidus), White-Throated Kingfisher (Halcyon smyrnensis), Lemon-Throated Warbler (Phylloscopus cebuensis) and the Philippine Pygmy Flowerpecker (Dicaeum pygmaeum) (Paguntalan & Jakosalem 2008). The discovery of the Cebu Hawk Owl (identified in the literature as Ninox philippensis spilonota) in five major forest patches (Tabunan, Argao, Dalaguete, Alcoy, and Boljoon) in Cebu (Jakosalem et al. 2012) has put the province into a much higher degree of conservation importance not only in the Philippine Islands but also worldwide. This study aimed to assess the effects of microclimate and microhabitat variables on the population density and distribution of C. cebuensis in the Argao Watershed Reserve.

    MATERIALS AND METHODSStudy Site. The Argao Watershed Reserve is geographically located between north latitudes of 9°50’ and 10°00’ and east longitudes of 128°28’ and 123°37’ on the island of Cebu in

    central Philippines (Fig. 1). It has an area of about 7,250 ha and is bounded in the north by the municipality of Sibonga, in the south by the municipality of Dalaguete, in the east by Bohol strait, and in the west by the municipalities of Dumanhug, Ronda, Alcantara, and Badian.

    The general topography of the area is steep, with rugged terrain ranging from 12% to 60% slope in any direction. The highest elevations ranging from 800 m above sea level (masl) to 1,000 masl are found at the headwaters of barangays Ablayan, Maloray, Manlapay of Dalaguete municipality, and in the barangays Santicon and Butong of Badian and Argao towns. On the other hand, the whole watershed is composed of 21 barangays, of which 13 barangays belong to Argao jurisdiction, seven barangays in Dalaguete, and only one in Badian municipality where most of the areas are located in the uplands (Community-Based Resource Management Project Report 1999).

    The entire watershed area has seven (7) rock formations including Pandan, Carcar, Calagasan, Butong, Linut-od, Barili, and Quaternary Alluvium. Four of those are resistant

    Figure 1. Map showing the location of the study sites (with map of Cebu Province below and Philippine map inset).

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  • to erosion, namely: Barili formation, Carcar limestone, Butong limestone, and Pandan formation. The remaining three rock formations are non-resistant to erosion, namely: Calagasan, Linut-od, and Quaternary Alluvium. The watershed area is located along narrow erosional window drifting northeast, with sequences of older steeply dipping clastic rocks of limestone and coal that strikes generally northward. The middle section of the watershed is a sequence of slightly metamorphosed sedimentary rocks with intermeddled flows. There are two predominant soil types in the study area, namely the Mantalongon clay loam (occupies 90% of the entire area) and the Lugo series (covers 10% of the area). These soils are derived from the weathered limestone rocks, calcareous, and sandstones. The area has slightly acidic to slightly basic soil with a soil pH ranging 6.5-8.2 (Community-Based Resource Management Project Report 1999).

    Southern Cebu where the study site is located belongs to climate type III based on the Modified Corona’s Classification. It is characterized by the absence of pronounced maximum rain period with a dry season lasting only from one to three months, either during the period from December to February or from March to May. This type resembles type I since it has short dry season.

    Argao Watershed has two types of forest cover, namely the naturally grown trees composed of indigenous or native species, plus the man-made or plantation forests that were formerly established by then Southern Cebu Reforestation Development Project (SCRDP) in the early 1970s. Some remnants of natural forest fragments are found at the peak of Mt. Lantoy and along the slopes of Argao River. Isolated forest patches are still present in barangays Canbantug, Panadtaran, Usmad, Tabayag, Conalum, and Cansuje where mother trees of Ipil Instia bijuga (Colebr.) thrive. Kuntze and Molave Vitex parviflora Juss. can also be found in these areas. Natural vegetation and plantation forests comprise 29% or 1,119.54 ha of the watershed area (Jakosalem et al. 2005).

    Site 1 (Barangay Tabayag). Site 1 lies 14 km west (UTM: 1094773 E; 559276 N) from the town of Argao, Cebu. It occupies the northwestern and southern mountain ridges of Argao watershed. It cuts across the watershed with steepest slopes (26-50⁰) to the top of the mountain range with gentle slopes of 9-15⁰ towards lower part. Most part lies between 6⁰ and 25⁰ in slope. It has a total timberland areas of about 277 ha consisting of 11.9 ha of mixed plantation forest and 13 ha natural vegetation with the total forest cover of 24.99 ha (Argao Local Conservation Area Management Plan 2014-2017). The elevation ranges from 130 masl to 600 masl, where the 26 point count circular plots were randomly established (sampling were concentrated in Mt. Lantoy forest). The site is dominated by some indigenous or native trees

    including Ardisia angustifolia, Palaquium glabrifolium Merr., Ficus pseudopalma, Mallotus philippinensis, Instsia bijuga, Gnetum gnemon, Vitex parviflora, Buchanania arborescens, Guioa myriadenia, Canarium asperum, Caryota rumphiana, Leukosyke capitellata, Garcinia binucao, Reutealis trisperma, Disopyros polyalthioides, and mixed plantation forest dominated by Swietenia macrophylla, Gmelina arborea, and Tectona grandis with the presence of climbing bamboo, Heteorospate elata, etc. The sampling site is bordered by cultivation, coconut plantations, plantations of non-indigenous trees, and scrubland, which is also used by local communities for grazing their livestock. Seasonal crops like corn, camote, onion, and carrots are planted in agricultural farms surrounding the forests (Jakosalem et al. 2005).

    Site 2 (Barangay Canbantug). This site is located 20 km southeast (UTM: 1092566 E; 556407 N) from the municipality of Argao. The topography of the area is moderately sloping with some portions that are quite steep. The 23 point count stations were established randomly on the forest patches with an elevation ranging 500-800 masl. It has a total timberland area of about 388 ha, comprised of 105 ha of plantation forest and 65 ha of natural forest with a total forest cover of 170 ha. The mixed plantation forests were planted with exotic species including Swietenia macrophylla (the most dominant), Gmelina arborea, and Delonix regia. Notable indigenous plants include Ficus chrysolepis, Ailanthus triphysa, Alstonia scholaris, Radermachera pinnata, Cratoxylum sumatranum, Mallotus mollissimus, Ptercymbium tinctorium, Litsea ampla, Diospyros multiflora, Morinda bracteata, Glochidion camiguinense, Dysoxylum arborescens, Micromelum ceylanicum, Palaquium cuneifolium, Arthrophyllum diversifolium, Neolitsea villosa, and Syzygium spp. There are also present threats to biodiversity in the area like kaingin, illegal cutting of trees for firewood, housing construction and mine timber, etc.

    Site 3 (Barangay Cansuje). Site 3 is located northeast (UTM: 1096083 E; 555974 N) and 15-20 km from the town of Argao. The 43 point count circular plots were randomly established on areas with elevation range of 500-800 masl. It has the biggest forest cover among the four sampling sites with the total coverage of 456 ha, of which 424 ha is composed of mixed plantation forest and 32 ha natural forest. This site was part of the reforestation project, the Southern Cebu Reforestation Development Project managed by the Department of Environment and Natural Resources, formerly Bureau of Forest Development back in 1970s. As such, most of the introduced species planted on the area were the following: Swietenia macrophylla (the most dominant), Gmelina arborea, and Tectona grandis, among others. Both strangler and erect figs in the Moraceae family were present on steep and rocky slopes, as well as

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  • along gullies or valley bottom. Grasses such as bamboos both climbing and erect, which are known to be a favorite habitat for Black Shamas, were also abundant in the area (Kennedy et al. 2000).

    The following are the common natural vegetation that were encountered during the survey: Palaquium glabrifolium, Leucosyke capitellata, Gnetum gnemon, Homalium samarense, Machilus curranii, Osmoxylon serratifolium, Neonaclea formicaria, Archidendron ellipticum, Ailanthus triphysa, Ardisia squamulosa, Ervatamia mucronata, Elaeocarpus grandifloras, Syzygium subfalcatum, Turpinia ovalifolia, Evodia bintoco, Syzydium vidalianum, Ormosia calavensis, among others. Some active and abandoned croplands were inside and on the forest edges creating canopy openings and open patches. There were also illegal cuttings of trees observed in the area for various purposes such as firewood and housing construction; the most rampant is for mine timber since there are coal mining areas within the site and also in the adjacent barangays.

    Site 4 (Barangay Usmad). This barangay is about 6 km northwest (UTM 1095236 E; 559753 N) from the town of Argao; so far, this is nearest site from the town proper. It has a total land area of about 487 ha (2.35% of the total land area of the municipality which is 20,754 ha) and 91 ha were classified as forestlands. There is no data available as to how many hectares are planted to exotic species. However, during the survey conducted there were plantations of mahogany, gmelina, and teak. The natural forest is consist of 34 ha of natural forest cover hence, total forest cover is pegged at 34 ha with only 31 ha classified as brush lands/ grasslands (Argao Forest Land Use Plan 2013). There were two habitat type being sampled in this study site, including pure and mixed forest. The former is composed of indigenous or native vegetation whereas for mixed, it consists of indigenous and exotic species. The 38 survey stations were laid on these habitats across elevations ranging 90-500 masl. Site 3 is part of the Argao-Dalaguete Watershed Forest Reserve declared by a Presidential Proclamation (No. 414, 29 Jun 1994). The common indigenous species encountered in the study site were the following: Micromelum ceylanicum, Azadirachta excelsa, Palaquium luzoniense, Ficus balete, Antidesma leucopodum, Guioa myriadenia, Osmoxylon serratifolium, Acalypha amentacea, Arthrophyllum diversifolium, Cratoxylum sumatranum, Neonauclea formicaria, Pometia pinnata, Artocarpus pinnatisectus, Palaquium luzoniense, Buchanania arborescens, Syzygium vidalianum, Ormosia calavensis, Ardisia pyramidalis, among others. Some threats to forest resources were observed including illegal cutting for housing construction, firewood, charcoal making, and mine timbers. Kaingin and conversion of forest lands to

    other uses, wildlife hunting, and collection of wild plants are the most prevalent in this area.

    Relationship between C. cebuensis Population Density and Microclimate and Microhabitat FactorsPopulation Counts of C. cebuensis. This study adopted the point count survey method following Bibby and colleagues (2000). A total of 130 circular point count stations with 20 m radius were established within the four sampling sites covering natural and man-made or mixed forest. Stations established were as follows: 26 plots in Site 1 (Brgy. Tabayag) with 4 hr and 10 min total observation time, 23 plots in Site 2 (Brgy. Can-bantug) with 3 hr and 50 min, 38 in Site 4 (Brgy. Usmad) with 6 hr and 10 min, and 43 plots in Site 3 (Brgy. Cansuje) with 7 hr and 10 min (Fig. 2). The geographic coordinates in each station was also taken (using hand held Garmin eTrex® 10 Global Positioning System receiver).

    In each station, observers waited for at least 2 min after arriving and then recorded the presence of Black Shama within a 20 m radius for 10 min. All target species seen or heard around the plot were recorded using play back mp3 player with portable speaker – an aid in establishing the presence of the target species around the station. For the species that are only heard, careful observation was undertaken so as not to include its sympatric congener (the Philippine Magpie-Robin Copsychus saularis) and other species that were also noted during the counting in all the sites. Carefully, the two species were distinguished from one another through their calls and their coloration. Black Shama (especially the male) has song varied series of melodious whistles, while Magpie Robins have calls quite varied, often imitative of other species, but all are clear, melodious, and repetitive whistles (Kennedy et al. 2000). C. saularis (both male and female) had also distinct color, with broad white wing patch that separates it from all shamas, while C. cebuensis especially adult (male) is bluish black in color, greyish brown for juvenile, and greyish black for a fully grown female species (Kennedy et al. 2000).

    The number of contacts with the species was recorded by following this pattern: one confirmed visual sighting and one single count each representing one single count. To avoid double counting the same species, the sampling stations were purposely laid 200 m apart from one another (Paguntalan & Jakosalem 2008). Other variables like start time, estimated radial distances to all target species encountered (using HP-800 laser range finder), number of contacts with the target species, height of contact, and the exact time when the contact happened were also noted. Target species that flew away from the immediate area were also recorded, and the radial distance made to their point of departure from the center of the survey station was

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  • then measured and recorded (Bibby et al. 2000). The same procedure was done for the target species that flush as the observer arrived at the station; however, these are not included in the record for the number of contacts unless it settled down to allow for radial distance estimation from the observer (Bibby et al. 2000). Observations were carried out from 0530 hr to 1000 hr and from 1530 hr to 1800 hr, since birds are more active during this period (Bibby et al. 2000). However, there were few observations with the species being recorded beyond the designated period of observation (1000-1530 hr). The survey was only undertaken during days with fair weather or sunny day (Bibby et al. 2000). No survey was made during rainy days since bird activities are expectedly suppressed during these days (Bibby et al. 2000).

    Data Collection Technique for Microclimate and Microhabitat Variables. The microclimate and micro-habitat variables were gathered directly or indirectly from the field, during which the point count sampling was conducted. These variables were categorized into the following: (a) physical, (b) vegetation features, and (c) microclimate variables. Physical variables included elevation, slope, exposure (see Appendix Table 1), and distance to the nearest available intermittent stream or valley bottom were measured directly on every point count station. Elevation was measured using hand held eTrex® Garmin 10 Global Positioning System (GPS) receiver (precision:

  • compass in the GPS receiver. Lastly, the distance of each sampling station to the nearest available intermittent stream or valley bottom was calculated indirectly using Global Information System (GIS) (Arc Info version 10) (nearest neighbor distance analysis). Table 1 presents the variables that were considered in this study.

    Vegetation features included canopy cover, shrub cover, and tree density. All these three variables were calculated every station. Canopy cover was measured directly in the field using a modified densiometer instrument (see Appendix 2 for detailed explanation), while shrub cover was taken using ocular estimate by proportional area (see Appendix Table 1 for detailed explanation). Tree density was calculated (see Appendix 1) using equation/formula (Bibby et al. 2000). The number of trees was measured through frequency counts, where the number of trees belonging to a certain diameter and height class was tallied and counted.

    Microclimate variables included temperature, relative humidity, and light intensity. Again, all these variables were taken every station. Temperature and relative humidity were determined using digital thermo-hygrometer. Light intensity was taken using Model EA30 Easy-View-Digital light meter.

    Estimating Population Density of Black Shama. For this study, the estimate of the population size or density was undertaken by the use of a distance software program (Distance version 6.2 Release 1; Thomas et al. 2010). Specifically, multiple covariate distance sampling (MCDS) analysis engine was utilized to model

    the detection function where covariates are being used (Thomas et al. 2010). For this study, the covariates were used including the estimated radial distance of the occurrence target species from center of the point count station and the number of contacts (Thomas et al. 2010).

    Regression Analysis. An enter method multiple regression analysis was applied to determine the relationship between the landscape variables (22 predictors were tested in the habitat level analysis and only 10 predictors were finally included in the sampling site) and population density of C. cebuensis using the following:

    Eq. 1 𝑌 = 𝑌 = 𝑏0 + 𝑏1𝑋1 + 𝑏2𝑋2 ⋅⋅⋅ + 𝑏𝑞𝑋𝑞 + 𝜀,

    where 𝑌 is the dependent variable (population density of C. cebuensis); 𝑋1, 𝑋2, ... , are the independent variables or predictors (landscape variables); 𝑏0, 𝑏1, 𝑏2, ... , 𝑏𝑞 are the partial regression coefficients of independent variables or predictors; and 𝜀 is the Random error. All statistical analyses were undertaken with SPSS 11.5 license at UPLB College, Laguna, Philippines.

    RESULTS AND DISCUSSION

    Effects of Microclimate and Microhabitat Variables on the Population Density and Distribution of C. cebuensisC. cebuensis Population Density Estimates for the Two Habitat Type (Mixed and Natural Forest). Table 2

    Table 1. List of microhabitat and microclimate variables considered in this study.

    HABITAT VARIABLES REFERENCESMETHODS OF

    MEASUREMENT

    (1) Physical features(a) Altitude/elevation(b) Slope gradient(c) Aspect(d) Distance/nearest streams/rivers

    Bibby et al. (2000)Bibby et al. (2000)Bibby et al. (2000)Bibby et al. (2000)

    GPS receiverAbney hand level

    CompassSpatial Analyst (GIS)(ArcInfo version 10)

    (2) Vegetation structures(a) Total height (TH)(b) Diameter at breast height (DBH)(c) Canopy cover(d) BA of trees/ha(e) Tree density/ha(f) % Shrub cover(g) Number of trees

    (1) Diameter classes(2) Height classes

    Bibby et al. (2000)Bibby et al. (2000)Bibby et al. (2000); Rosli et al. (2012)Bibby et al. (2000)Bibby et al. (2000)Rosli et al. (2012); Posa & Sodhi (2006)Rosli et al. (2012); Posa & Sodhi (2006)Rosli et al. (2012); Posa & Sodhi (2006)Rosli et al. (2012)Rosli et al. (2012)

    Haga altimeterDiameter tapeDensiometer

    Computation/equationComputation/equationComputation/equation

    Ocular observationFrequency/Counts

    Tally/CountsTally/Counts

    (3) Microclimate (a) Temperature (b) Relative humidity (c) Light Intensity

    Rosli et al. (2012); Posa & Sodhi (2006)Rosli et al. (2012); Posa & Sodhi (2006)Rosli et al. (2012); Posa & Sodhi (2006)

    Digital-Min/Max Thermo-hygrometer

    Model EA30 Easy-View-Digital Light Meter

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  • presents the estimated population density of C. cebuensis (using DISTANCE 6 release 2 software program) for two habitat types, where mixed forest had 52 and 53 individuals-ha−1 for natural forest having the same coefficient of variation (CV) of 10% at 95% confidence interval. It is noted that these two habitat types or strata have more or less equal in the density of population per unit area.

    This suggests that C. cebuensis had already adapted to this type of habitat conditions in the watershed area where they inhabit. Previous studies have reported that Black Shama inhabit various types of habitat including scrub, cut-over forests, plantations, undergrowth of secondary tracts along steep ravines, and bamboo groves (Gonzalez & Rees 1988; Dickinson et al. 1991; Magsalay 1993; Brooks et al. 1995a; Collar et al. 1999; Jakosalem et al. 2005). These findings further showed that Black Shama are still widely distributed among the remaining forest habitat patches within the Argao watershed despite the area being highly fragmented, degraded and highly disturbed. Previous study with Black Shama also complemented this finding that the species prefers forest habitats and may only tolerate degraded habitats, as there are very few remaining forest patches in Cebu (Jakosalem et al. 2005). It can be observed that the persistence of C. cebuensis to a variety of habitat types has made this bird species distribution may be more widespread all throughout the watershed area.

    C. cebuensis Population Density Estimates at Sampling Sites. Among the sampling locations, Barangay Cabantug and Barangay Cansuje had the highest pooled population density estimate of C. cebuensis with 118 individuals-ha−1 followed by Barangay Usmad with 114 individuals-ha−1, and the lowest is Barangay Tabayag with 81 individuals-ha−1 (Table 3). It can be observed that though Barangay Canbantug and Barangay Cansuje have the same population density estimates, but they had different %CV of 40% and 18%, respectively. It was observed further that the the number of contacts negatively influences the %CV. According to Bibby and colleagues (2000), for a distance sampling method to be adapted especially in point count survey, it needs to have at least 80-100 individual contacts in order to achieve more reliable estimates of the density of population for certain organism under consideration. As far as this study is concerned, it had satisfied this requirement because the number of contacts with Black Shama was 130 for all the habitat types as well for the

    sampling sites included. Based on these findings, it can be inferred that C. cebuensis are still widely distributed among the forest fragments or habitat patches remaining in Argao watershed. These findings also corroborates with the findings of Jakosalem and colleagues (2005), which suggest that subpopulations of Black Shama are present in consider-able number especially in Nug-as forest in Alcoy, Cebu and in Argao municipality. Though a century ago, this endangered bird species was pronounced as “very rare” on Cebu (Bourns & Worcester 1894; McGregor 1909-1910) and as the scarcest of the Philippine shamas, with few in number and very low population (Hachisuka 1936).

    Regression Analysis between Microhabitat/ Microclimate Variables and Population Density of C. cebuensis for the Two Habitat Type (Mixed and Natural Forest). Table 4 presents the results of regression analysis between the population density of C. cebuensis at habitat level. The final model shows that: adjusted R2 = 0.345, F20, 107= 4.093, p

  • terrestrial insectivorous birds just like the C. cebuensis were sensitive to forest edge and could indicate the quality of forest interior habitat associated with high humidity, dense canopy cover, and deep litter depth (Moradi et al. 2009; DesGranges & Morneau 2010). A study of upper storey birds also in Malaysia showed that bird responses are significantly correlated with environmental variables associated with various distances from the forest edge

    (Rosli et al. 2012). The effects of anthropogenic land use on the natural habitats at Subic Bay Forest Reserve have been studied and its findings complemented this study, which showed that forest bird species are positively correlated with vegetation variables such as canopy cover, tree density, height to inversion, and ground cover (Posa & Sodhi 2006; Cintra & Naka 2012). Results further revealed that majority of the bird contacts were sensitive to canopy

    Table 3. Pooled density estimates of population density of C. cebuensis in four sampling locations.

    SAMPLING LOCATIONS (BARANGAY)

    POOLED DENSITY ESTIMATES (D)

    COEFFICIENT OF VARIATION

    (CV-%)

    DEGREES OF FREEDOM (df)

    95% CONFIDENCE INTERVAL

    Tabayag 81 38.98 24.24 37.312 176.07

    Canbantug 118 40.52 22.47 52.860 265.87

    Usmad 114 20.42 42.18 75.921 171.64

    Cansuje 118 18.21 50.18 82.514 170.49

    Table 4. Results of regression analysis between population density estimates of C. cebuesis at habitat level (with 20 predictors or variables included).

    MODELPREDICTORS(CONSTANT)

    CODE

    UNSTANDARDIZED COEFFICIENTS

    STANDARDIZED COEFFICIENTS SIG.

    BSTD.

    ERROR BETA

    (Constant) .083 44.827 .999

    (1) Altitude/Elevation AL .000 .003 .014 .882

    (2) Slope SLP .028 .029 .075 .331

    (3) Distance from nearest stream DFNS -.001 .001 -.059 .468

    (4) Temperature TEM .437 .293 .146 .139

    (5) Relative humidity RH .245 .053 .400 .000

    (6) Light intensity ILUX -8.959E-05 .000 -.021 .805

    (7) Tree basal area TBA -9.269 1.566 -.660 .000

    (8) Canopy cover TCPY .021 .006 .261 .001

    1 (9) Shrub cover SHBC .073 .043 .156 .090

    (10) No. of trees (dbh ≥10-19); NTB -.304 1.345 -.019 .822

    (11) No. of trees (dbh ≥20-29) NTC -1.031 4.094 -.380 .802

    (12) No. of trees (dbh ≥30-39) NTD -.525 4.141 -.130 .899

    (13) No. of trees (dbh ≥40-49) NTE -.808 4.106 -.154 .844

    (14) No. of trees (dbh ≥50-59) NTF -.057 4.126 -.007 .989

    (15) No. of trees (dbh ≥60 cm) NTG -.312 4.421 -.015 .944

    (16) No. of trees (

  • loss and requires 60% canopy cover and higher in order to maintain a good environmental condition for the birds. A study in Idaho, CA, US revealed that tree canopy cover was so important for habitat selection of 86 mammal and avian species (Joshi et al. 2012).

    Tree basal area had negative high significant correlation with C. cebuensis population density with coefficient (beta) value of -0.660 and a p-value of 0.000 significant at 0.01 level. This finding indicates that with greater tree basal area on the point of survey, the population density of C. cebuensis may be possibly lesser. It was observed during survey that most sampling stations were not containing considerable number of big trees. However, there were few stations contained appreciably big diameter trees, which connote greater basal area. The study on insectivorous birds (Magpie Robin was included in the study) and environmental factors in Malaysia’s tropical rainforest showed that terrestrial insectivores were sensitive to forest edge and could indicate the quality of forest interior habitats associated with high humidity, dense canopy cover, and deep litter depth (Moradi et al. 2009). Further, the findings of this study indicated that basal area is not significantly correlated with all the insectivorous birds included in the analysis (Moradi et al. 2009).

    Regression Analysis between Pooled Population Density Estimates of C. cebuensis and Landscape Variables for Sampling Sites. Based from the multiple linear regression analysis (using enter method), the results have shown a final model of: adjusted R2= .212; F10,

    119=4.474, p< 0.000 with only 10 predictors included in the final analysis. This indicates that the model has accounted only 21.2% of the variation of population density of C.cebuensis, which is lower by 13.3% compared to what is accounted for in the regression done at the habitat level. Table 5 presents the results of the regression done at this level.

    It can be observed that there are four predictors have explained the behavior of the population density of C. cebuensis, namely: a) elevation, b) slope, c) canopy cover, and d) shrub cover.

    Elevation has positive high significant correlation (beta) with population density of C. cebuensis with standardized coefficient of 0.398 and with p-value of 0.000, significant at 0.01 level (Table 5). This means that with increasing elevation, the density of population of C. cebuensis will likely increase (sampling confined at the elevation range of 100-800 m, wherein the highest elevation was recorded at site 2 (Brgy. Canbantug). According to Bhatt and Joshi (2011), variations in the number of bird occurrences (Oriental Magpie Robin included) along elevation gradient in the natural and urbanized habitats in western Himalaya, Nainital district of Uttarakhand, India found that bird species richness (BSR) varied considerably with elevation. This difference in BSR among study sites could be due to elevation, and vegetation differences associated with elevation and not caused by the presence of a group of mid-altitude specialists. It has been observed that in all the areas being sampled, elevation may not be the strong

    Table 5. Results of the regression analysis between pooled population density estimates in four sampling sites (with 10 predictors included in the analysis).

    MODEL PREDICTORS

    UNSTANDARDIZED COEFFICIENTSSTANDARDIZED COEFFICIENTS SIG.

    CODE BSTD.

    ERROR BETA

    (Constant) 85.333 27.538 .002

    (1) Elevation ELEV .030 .007 .398 .000

    (2) Slope SLP -.148 .068 -.178 .032

    (3) Temperature TEM .651 .680 .097 .341

    (4) Relative Humidity RH .029 .115 .022 .799

    1 (5) Light Intensity ILUX 6.542E-05 .001 .007 .938

    (6) Tree Density TDEN .007 .015 .040 .626

    (7) Canopy Cover TCPY .186 .091 .177 .043

    (8) Shrub cover SHBL -.157 .078 -.165 .047

    (9) Diameter-at-breast- height DBH -.106 .241 -.046 .660

    (10) Total Height TH -.466 .491 -.101 .345

    F (10,119) = 4.474 Sig. of F = .000 R2 = .273 Adjusted R2 = .212

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  • predictor of C. cebuensis population density, considering that the survey confined generally at lower elevation.

    In this study, the findings suggest that vegetation structure appeared to be the strongest predictor for C. cebuensis population density, with canopy cover highly correlated with the latter. Mallari and co-workers (2001) noted that Philippine birds are lowland forest specialists, which disappear or become much rarer above certain elevations (generally 1,000-1,500 m).

    For slope and shrub cover, it is negatively correlated with population density of C. cebuensis with coefficients of -0.178 and -0.165 and with values of 0.032 and 0.047 significant at 0.05 level, respectively. These findings indicate that with increasing slope and shrub cover, the population density of C. cebuensis will likely decrease. It can be observed that among the areas being sampled (particularly in site 4 and site 2) with higher shrub cover and lower canopy cover, the number of contacts with C. cebuensis is lesser. A separate study of Carrascal and Diaz (2006) found out that the most essential habitat structure variables related to bird distribution were the density of young and mature oaks: a thick undergrowth of thin oaks negatively influenced total bird abundance and species richness. The impact of this variable towards the distribution of the target species appeared to be that there is certain amount of shrub cover that they thrived more favorably and beyond which, the distribution seemed to decrease.

    For slope, it can be observed that in all the areas being sampled with higher slope, the number of contacts with target species is lower. This effect could be attributed to the altered vegetation structures, especially those brought about by a steeper or higher slope gradient. Trees and other plants growing on ridges appeared to be more stunted than those growing in valleys and/or median slope or at lower slope, as observed in this study. However, this habitat condition may not only be the factor of slope but rather of vegetation type, species composition, geology, and soil moisture (Farina 1997; Whittingham et al. 2002). In cases where steeper slopes is associated with higher altitude, frequent periods of harsh weather generally strike the higher mountainous areas, affecting to a lesser degree lower elevation; hence, the number of contacts with the target species declined (Carrascal & Diaz 2006; Pagaduan & Afuang 2012). A separate study conducted in Alcoy, Cebu corroborated this finding, which suggests that Black Shama was also encountered more in valley-bottom forests than on ridge-top forests, which is associated with higher slope (Jakosalem et al. 2005).

    Lastly, for canopy cover, it had positive significant correlation with C. cebuensis population density with coefficient of 0.177 and a p-value of 0.043, which is significant at 0.01 level. It can be observed that the

    regression test result for this variable is consistent for both habitat and at sampling level (pooled population density estimate). It can be further inferred that for Black Shama, being an understorey and insectivorous bird species, canopy cover is one of the vital environmental variable for it to persist in a given habitat.

    CONCLUSIONS In regression analysis, there are only three out of 20 and four out of 10 parameters that have been able to predict or explain the behavior of the population density of C. cebuensis at habitat and sampling site levels. Predictors that are positively highly significant at the habitat level were the following: (a) relative humidity (0.400, 0.01 < 𝑃 value = 0.000) and (b) canopy cover (0.261, 0.01 < 𝑃 value = 0.001) while (c) tree basal area is negatively highly correlated (−0.660, 0.01 < 𝑃 value = 0.000). At sampling site, elevation has high positive significant correlation (0.398, 0.01 < 𝑃 value = 0.000) with C. cebuensis population density, and canopy cover has positive significant correlation (0.177, 0.05 < 𝑃 value = 0.043), whereas slope and shrub cover have negative significant correlation (−0.178, 0.05 < 𝑃 value = 0.032 and −0.165, 0.05 < 𝑃 value = 0.047). Based on the final model and given the two levels of analysis, at habitat level, results have shown that 34.5% of the variance soft the population density of C.cebuensis have been accounted for, while at the sampling site level it accounts only for 21.2%. Study suggested that regression analysis at habitat level is better than same analysis at sampling site. Study concludes with a series of sound policies and management recommendation to preserve Argao watershed.

    Policy Measures to Protect C. cebuensis Native Habitats. Integrating the use of indigenous trees species in rehabilitation and reforestation programs – whether it is undertaken by public agencies or private entities – within the study site is important to preserve native habitat for C. cebuensis. This must take into account the remaining forest within the watershed area, especially for Site 4 (Brgy. Usmad) where habitat patches are highly disturbed by human activities and some portions of sites 1, 2, and 3. Promoting and adopting the habitat or landscape approach in rehabilitating degraded habitats. This approach, however, focuses on the relationship at various scales from species up to landscape. Each and every element or patch is taken into account as a basic unit of the entire system.

    Management Aspect. Management and rehabilitation of remaining forest habitat patches within Argao watershed especially for the four sampling sites (sites 1, 2, 3, and 4) should be based on the findings of the regression analysis conducted in this study. Institute connections on

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  • isolated patches, mainly through corridor establishment using riparian forest, is an excellent option as patches connection in this case is imperative. There is a need to rehabilitate riparian vegetation, especially those that are highly degraded and sparsely stocked with vegetation like sites 4 and 2.

    Further Research on C. cebuensis. Further research should be explored on the clear and present threats on the forest resources, which would lead changes in microclimate and microhabitat factors that can ultimately affect C. cebuensis distribution. Also recommended are follow-up studies on the effect of patch area on the population density and/or abundance of the target species covering the four sampling sites. This study was able to survey selected forest habitat patches within AWR. However, the effect of the patch area with the population density of C. cebuensis has not been explored.

    ACKNOWLEDGMENTThe study received financial support primarily from the Department of Science and Technology, Science Education Institute (DOST-SEI) – Accelerated Science and Technology Human Resource Development Program (ASTHRDP), Philippine Council for Aquatic, Agriculture, Forestry and Natural Resources Research and Development (PCAARRD), the National Research Council of the Philippines (NRCP), and the whole composition of the guidance committee: Chaired by Dr. Rex Victor O. Cruz (Watershed/Climate Change) and the rest of members: Dr. Nathaniel C. Bantayan (GIS), Dr. Diomedes A. Racelis (FRM), Dr. Inocencio E. Buot, Jr. (Biodiversity), and Leonardo M. Florece (Ecosystem) for which the author was so grateful.

    NOTE ON APPENDICESThe complete appendices section of the study is accessible at http://philjournsci.dost.gov.ph

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  • Appendix I. Detailed explanation of the methods of measurement of some variables (e.g., slope, exposure).

    Variables Methods of Measurement

    (1) Slope

    (2) Exposure or Aspect

    (3) Elevation

    (4) Shrub cover

    Abney hand level was used in measuring this variable wherein the person assigned to get the measurement positioned himself on the upper ground with respect to the plot center and the angle of inclination of a line was measured from his position to a certain target wherein the line of sight follows the slope direction. The slope reading was taken from the graduation. For this study, slope reading used is in %.

    For this variable, the instrument used was the built-in compass in the etrex 10 Garmin GPS receiver, the measurement or reading of the general orientation for each point count station was obtained through direct reading from the compass. The person assigned for taking down measurement stood still with the hand-held GPS receiver and waited for a couple of minutes until the precision reached below ±5 for reliable results. Once, the desired GPS precision was attained subsequently the final reading was then obtained.

    The measurement in the elevation for this study was accomplished through the use of the etrex 10 Garmin GPS receiver. The person assigned in getting the reading stood still for a while until the GPS receiver attained a precision of below ±5. Once the target precision was attained the reading or measurement was finally undertaken. For this study, the unit of measurement being used is in meters above sea level.

    This variable was determined through ocular estimate of the shrub coverage for each point count station. Basically, this was undertaken by means of an area proportion. This is accomplished through dividing the station into four quarters and each quarter is equivalent to 25%. The estimate was done progressively starting on the first quarter depending on the shrub coverage and the final estimate was made by cumulatively adding the previous estimates.

    G, KHAIRULMAZMI A. 2012. Response of uperstory birds to the environmental variables at different distances from the edge of an isolated forest reserve in Malaysia. Asia Life Sciences Journal 21(1): 65-84.

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    VARESTEH HM, ZAKARIA M, MOHD A, YUSOFI E. 2010. Insectivorous birds and environmental factors across an edge-interior gradient in tropical rainforest of Malaysia. IZR 6: 131-145.

    VIRKKALA R, HEIKKINEN RK, LEIKOLA N, LUETO M. 2008. Projected large-scale range reductions of northern-boreal land bird species due to climate change. Biodiversity Conservation 141: 1343-53.

    WHITTINGHAM MJ, PERCIVAL SM, BROWN AF. 2002. Nest-site selection by golden plover: why do shorebirds avoid nesting on slopes? Journal of Avian Biology 33: 184-190.

    YAHNER RH, SCOTT DP. 1988. Effects of forest fragmentation on depredation of artificial nests. Journal of Wildlife Management: 2: 158-161.

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  • Appendix II. Procedure for using improvised densiometer.

    Appendix III. Procedure for using improvised densiometer.

    Figure 0.0. Homemade densiometer.

    Figure 0.1. How to use improvised densitometer.

    Figure 0.2. Directions on considering plus (+) and minus (-) canopy readings.

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