Bird Diversity and Structure in Different Land-use types in Lowland [PDF]

Bird Diversity and Structure in Different Land-use types in Lowland south Central Mindanao, Philippines

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Krizler C. Tanalgo*, John Arislyn Pineda, Maricel Agrvante and Amerol Zabide

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Department of Biological Sciences, College of Arts and Sciences, University of Southern Mindanao,

Kabacan, North Cotabato, 9407, Philippines 2

Department of Secondary Education, College of Education, University of Southern Mindanao, Kabacan,

North Cotabato, 9407, Philippines

*Corresponding author: [email protected]

Abstract: Birds are crucial in maintaining ecosystem balance by providing various ecological services. The diversity and the feeding guild of birds in different land-use types were investigated in south central Mindanao to elucidate the effect of disturbance and habitat modification to bird community. Point count method was employed to identify birds in three habitat types: i) agroforest, ii) ricefields, and iii) roads and heavily disturbed area. A total of 1114 bird sightings were recorded belonging to 33 species and 24 families. Of these, three were Philippine endemic and five were migrant species. Among all habitat types, highest species diversity was determined from agroforest (1/D= 16.148) and the least was recorded from road and heavily disturbed habitat. Greater species composition similarity was found between agroforest and ricefields than to areas with high disturbance level such as roads. The characteristic of vegetation and availability of food resource may play a vital factor to the diversity of birds in every habitat as evidenced by high species richness of frugivores and insectivores in agroforest and rice fields respectively, where food source are largely available in both habitat. Streptopelia tranquebarica, was noted as new Island record in Mindanao and sighted particularly in ricefields. Consequently, this study indicates that habitat modification may alter avian diversity and structure and the maintenance of vegetation as of food resources and habitat in land-use system are essential strategies to conserve native and important bird species in lowland south Central Mindanao.

Keywords: Agroforest, Avifauna, Conservation, Feeding guild, Frugivores

INTRODUCTION

The Island of Philippines is admittedly one of the richest countries in the world as far as biodiversity is concerned. The Philippine tropical rainforest is regarded as one of the richest in Southeast Asia, with exceptional species diversity and high number of endemic species (Heaney 1993). However, transformation of tropical rain forest to agricultural lands has resulted in the local and regional extinction of many species (Myers 1988). Lowland forest in the Philippines has decreased by about 90%. Roughly 94% of the Philippine land area was once covered by forest, and reduced to 40% at the end of World War II, and current estimates to forest cover range from 25% to less than 20% (Utzurrum 1991; Forest Management Bureau-DENR, 2003; Carandang, 2005). The vast Archipelago of the country harbors more than 700 species of birds known to exist with increasing number due to numerous sampling and survey expeditions. The natural habitat of most birds throughout the country is tropical forest. The 67% of Philippine birds spend their life or part of their life in forest. However, much of the tropical forest in the Philippines has been cleared out for logging, mining, agriculture, industrial and development purposes (Birdlife International 2014). Birds are present in various habitat types and among the important groups that play a very vital role both in the structure and function of the ecosystem by providing various ecological benefits such as seed dispersal, facilitating forest restoration (Lozada et al. 2007), pollination of many tropical plant species, and pest-control services by consumption of insects (Philpott et al. 2009; Sekercioglu 2012) and small rodents that devastates hectares of agricultural products. Thus, birds are an ideal group to examine for ecosystem service valuation (Weeny et al. 2011). Although less than 1% of the world’s bird species primarily prefer agricultural areas, nearly a third of all bird species occasionally use such habitats (Sekercioglu et al. 2007). Some agroecosystems can also harbor a substantial portion of the biodiversity of the original land cover (Vandermeer & Perfecto

1997) and can buffer and complement protected areas (Curran et al. 2004; Schroth et al. 2004). Whilst, areas planted with rice (Oryza spp.) are also used by a wide variety of bird species during the nongrowing season and play an important conservation role in many parts of the world (Elphick et al. 2010). Environmental effects on birds are typically assayed by recording changes in population density, abundance, or distribution in a species habitat types (Temple and Wiens 1989). The objective of this study mainly deals with the determination of avifaunal species assemblage and status in different landuse type in south Central Mindanao, Philippines. This paper aims to: 1) identify bird species up to the lowest possible level of taxonomic classification in three different land-use types (agroforest, ricefields and roads), 2) determine and compare species diversity, conservations status, and endemism, and 3) relate species diversity to the extent of disturbance in different habitats.

METHODOLOGY

The Study Site The study of the avifaunal diversity and feeding guild in varying habitat was conducted in a 1024 hectare campus of University of Southern Mindanao, in south central Mindanao (Figure 1). The study site was chosen for its variety of habitat types present that includes agroforest, orchard, ricefields and heavily disturbed habitats (roads + buildings), the uniform elevation along all habitat also makes it a good sampling site, thus elevation as factor on bird diversity was excluded from the analysis. Elevation of the o

study sites ranges from 33 to 60 masl with annual mean temperature of 27.48 C and mean rainfall 1980 to 2500 mm/year (World Climatic Database, 2014). Each habitat types are unique in terms of floristic and level of disturbance. Each land use types were described accordingly.

Agroforest Agroforest habitat (7° 6′ 36.558ʺN, 124° 50′ 51.331ʺ E) is characterized by a former secondary forest mixed with vegetation dominated by fruit bearing trees like Lanzones (Lansium domesticum), Pomelo (Citrus maxima), Durian (Durio sp.), Rambutan (Nephelium lappaceum), Chico (Achras zapota), and

Papaya (Carica papaya). Corn (Zea maize) and Banana (Musa paradisiaca) are present at the edge of orchards like in Chico and lanzones. Cogon (Imperata cylindrica) was covering some patches of the area especially the edges of the cornfields while Mahogany (Swietenia mahogani) was noted to cover some parts of the manmade paths.

Rice fields The rice field habitat (7°7’10.324” N, 124°49’22.979”E) is surrounded oil palm (Elaeis guineensis) coconut (Coco nucifera), Acacia (Samania saman) and other vegetations like shrubs, ferns, and grasses. Other areas of rice fields are dominated corn (Zea maize), and mango tree (Mangifera indica). Three cropping season is established every year with 2.5-3 months of growing season. The sampling period started from the harvest season and ended during early-field preparation were field flooding and soil plowing were observed. During the growing season, pesticide and herbicides were used to prevent insects and weeds from harming the growth of the crop.

Roads and Heavily Disturbed Heavily disturbed habitats (7° 6' 59.784''N and 124° 49' 59.073''E) primarily represented by roads and areas with infrastructures such as buildings, parks, canteens, hospital buildings, dorms and cottages inside the campus where human disturbance is very high and visible. Vehicles and motorcycles are also found in the study site. Trees such as Mahogany and Oil palms (Elaeis guineensis) were planted on road edges dominated by tall grasses such Cogon (Imperata cylindrica) and other species of grasses and sedges.

Sampling method Birds were observed in their habitat through point count method as described by Sutherland et al. (2004). At least 15 points were established along existing manmade or natural trails in each habitat with about 200 linear distance. Every point was observed for 20 minutes starting at 5:30 to 7:30 in the morning and 3:30 to 5:30 in the afternoon where the birds are usually active. All birds perceived visually and through calls within 30 m of the observer were listed. The researchers walked in a slow and constant speed to

ensure proper and non-biased observation.. Binoculars, tablet, DSLR camera and photographic field guides were used in the observation of sighted birds. All observations were recorded on the field journal. Sighted birds were identified based on their morphology, behavior and call based on Kennedy et al. (2000) and Fisher and Hicks (2006). Ecological status of identified birds were determined as to endemism using the same field guides. Conservation status were determined using the data provided by the International Union for the Conservation of Nature (IUCN 2014). Published literature guides were used to determine the feeding guilds of the identified species.

Birds Species Diversity The relative abundance of bird species (%) were calculated using the equation N/n (where: N is species’ (x) total number of the individuals captured and n is the total number of all species). Relative abundance of species and relative abundance of all species per each land-use type were measured. Avifaunal species diversity at each were compared using the reciprocal form of Simpson’s index (1/D), 1/D = pi

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(where: 1/D =reciprocal of Simpson’s D, pi = abundance of common genera) and calculated using 2

Biodiversity Pro 2.0 software (McAleece et al. 1997). Bray-Curtis (single-link) cluster analysis was further used to determine percent similarity in diversity and foraging structure along different land-use types.

RESULTS

Diversity of Birds along different Land-use types Point-count method was employed to identify bird species from three habitat types: i) agroforest, ii) ricefields, and iii) roads and heavily disturbed. A total of 1114 individual sightings belonging to 33 species under 24 families (Table 1). Of the three habitats, agroforest contains the highest percentage of individual sightings comprising the 44.16% of the total individual sightings, followed by ricefields (40.57%) and roads (15.26%). In agroforest, a total of 497 individual belonging to 27 species were recorded. Pycnonotous goiavier was the most recorded species representing the 13% of the total sightings, followed by Hirundo

tahitica (11.79%), and Geopelia striata (7.52%). In ricefields, a total of 452 individual sightings was recorded representing 25 bird species. Species such as Diceaum australe and Muscicapa sp. were only recorded in agroforest. Ardeidae and Columbidae have the highest family represented with 3 species (11%). Followed by family Estrildidae and Hirundidae with 2 species (7%) and the rest of the families were represented by single species (3%). Among all species recorded, Hirundo tahitica (16.37%) is the most abundant species recorded inhabiting the area. The area with least individual and species recorded was in heavily disturbed habitat represented by roads. A total of 170 sightings and 22 species was recorded in the area. Columbidae was the most species rich family with four species namely Chalcophaps indica, Geopelia striata, Phapitreron amethystinus, and Spilopelia chinensis. Two species, Collocalia esculenta and Aplonis payanensis were the most sighted species representing 14.70% of the total recorded individuals. Bird species diversity among habitat types was measured by the species dominance. The reciprocal form of the Simpson’s diversity index (1/D) was employed to measure the diversity of birds recorded from three land-use types. The agroforest recorded the most diverse habitat (1/D=16.146) followed by ricefields (1/D=13.934) and roads and heavily disturbed habitat (1/D=12.579). This result was further supported by the result on community similarity among habitats. Using the Bray-Curtis cluster analysis (Figure 2), it was found out there is greater similarity between agroforest and ricefields in terms of species composition compared to area with high disturbance and human encroachments such as roads. The result of this investigation also showed that as the vegetation structure changes and disturbance increased the abundance of bird sighting also decreased. Furthermore, fifteen species (45.46%) namely Apolonis payanensis, Artamus leucorynchus, Collocalia esculenta, Corvus cf. macrorhynchos, Geopelia striata, Halcyon chloris, Hirundo tahitica, Lanius cristatus, Lonchura atricapilla, Padda oryzivora, Passer montanus, Pycnonotous goiavier, Rhipidura javanica, Stigmatopelia chinensis and Tachycineta bicolor were common in three habitat types. In 33 species recorded from different habitat types, three species were Philippine endemic namely, Phapitreron amethystina, Centropus viridis and Dicaeum australe. C. viridis is a Philippine endemic caucal, it was only recorded in two habitat types –roads and agroforest. This species can be found in a wide varieties of habitats from grassland, mixed cultivations, second growth and forest up to

2000 m, alone or in pair. Caucals are shy and hard to sight except when they are perching in open or top of the grasses or small trees. It has a floppy flight and skulks through dense vegetation (Kennedy et al. 2000). The columbid, P. amethystina is an endemic dove species in the Philippines. This dove species can be found in lowlands but prefers middle and higher elevations from 500 to 2000 masl in primary and secondary forest (Kennedy et al. 2000). In the study site, it was recorded in flocks or in pair in trees in roads and deep inside the agforeest. The Philippine endemic flowerpecker D. australe was only recorded foraging in agroforest. According to Kennedy et al. (2000), this species dwells in the canopy of forests, forest edge, second growth, and shrubs in open countries in fruiting tress; singly or in groups and in mixed flocks usually below 1000 masl. Based on the bird sightings, no endemic species was recorded from the ricefields. However, wetland and migrant species such as Ardeola speciosa, Bubulcus ibis, Egretta garzetta and Tringa stagnitilis were recorded in foraging in ricefields. Noteworthy is the occurrence of T. stagnitilis, a rare migrant species in the Philippines. This species was observed in flock feeding on many injurious pests in the paddy of rice fields. Another noteworthy findings from this study is the new Island distribution record of Streptopelia tranquebarica where it is only known to occur in Bataan, Calayan, Lubang, Mindoro and Luzon areas (Kennedy et al. 2000) but recorded in the study site particularly foraging in ricefields. The conservation status of bird species was assessed using the latest information provided by the International Union Conservation of Nature (IUCN) redlist. Among all species recorded, only single species was determined threatened, P. oryzivora was considered as Vulnerable by the International Union for the Conservation of Nature Red List (2014). According to IUCN, this species is a native endemic to the islands of Java, Bali, and probably Madura, Indonesia, although it has been widely introduced and increasing population but due to trapping for the domestic and international cage-bird trade has probably been extensive for centuries, peaking in the 1960s and 1970s, and is the main cause of the decline. Its flocking tendency, particularly at roost sites, renders it especially susceptible to mass trapping. Ironically, even feral populations, originally introduced through trade, have subsequently been decimated for the same reason. In the study site, this species was recorded in all habitat types.

Avifaunal foraging structure Feeding guild is a group of species that exploit the similar kinds of food resources in a habitat. It is usually based on the kind of food they eat and it helps to determine the feeding behaviors of different bird species and the availability of food sources in the study area. Foraging guilds may be useful tools for examining changes in species-rich communities because their functional organization can be investigated even if they do not share any species (Terborgh and Robinson 1986). Five types of feeding guild was identified from the study area: carnivore, frugivore, insectivore, granivore, and nectarivore. All three habitats were dominated with insectivore species with 36% in agroforest, 30% in rice fields and 24% in heavily disturbed habitat (Figure 3). Insectivore species dominated the whole community in all habitat types. Artamus leucorynchus, Collocalia esculenta, Geopelia striata, Hirundo tahitica, Lanius cristatus, Rhipidura javanica, and Tachycineta bicolor were the most common insectivore species known to occur in the study site. Greater similarity in feeding guild structure between agroforest and ricefields with 79.98% similarity compared to that in roads (51.76%) was revealed (Figure 4). Frugivorous bird species was most abundant in agroforest and road with five species (15%) each habitat. In agroforest, the most abundant frugivores were Pycnonotous goiavier and Aplonis payanensis, these species were observed to forage in fruiting trees with small and ripe fruits. In roads, A. payanensis was the most abundant frugivore species constituting the 14.75% of the total sighting, this species was observed perching in wooden post beside the roads and other infrastructure in urban site. The least number of frugivore species was recorded in rice fields with only two species (6%). Carnivore species were mostly recorded from ricefields, where the most abundant carnivorous species were Egretta garzetta (8.85%) followed by Bubulcus ibis (6.64%) and Halcyon chloris (4.42%). Large carnivore species Haliastur indus and Corvus macrorhynchos were noted hovering and foraging in small vertebrates in rice fields such as rodents. Two species of carnivores were recorded both in agroforest and roads, H. chloris (5.9%) and E. garzetta (3%) were the most abundant carnivore observed in agroforest and roads respectively, however, the observation of E. garzetta may be accidental record in roads because of its single record during the sampling duration. Species from the family Estrildidae dominated most of the granivore species. Passer montanus was the most abundant and dominant species in rice fields, this was followed Lonchura atricapilla and Padda oryzivora, all of these

species are present in three habitats. Three dove species, Geopelia striata, Stegmatopelia chinensis and Streptopelia tranquebarica were also granivore species recorded. Moreover, only two species of nectarivorous species were recorded. Dicaeum australe was only recorded from agroforest and Nectarinia jugularis was recorded both in agroforest and roads, and both species were absent in rice fields.

DISCUSSION The result of this study suggest that higher bird diversity is found in agroforest than those in ricefields and roads. The result of this study conforms to the conclusion of Azman et al. (2011) in bird structure in different habitat types, that bird diversity is higher in areas to high vegetation diversity such as primary and secondary forests. The agroforest examined on this study is described by mixture of tall, large, and fruit bearing trees with wide canopy cover and the greater bird diversity of birds in this habitat may be influenced by the presence of important resources for birds to tolerate the disturbance brought by land use. Most of the species identified in this habitat were resident species with few forest dependent species, and though it contains endemic species, it is still very low compared to forest habitats in the region (see Achondo et al. 2012; Achondo et al. 2014). Of all bird species recorded, Pycnonotus goiavier was the most abundant species, this species belonging to family Pycnonotidae are important avifaunal group in forest restoration due to their efficient seed rain activity in lowland forest types (Sritongchuay et al. 2014). The general result of this study agrees with the findings of Harvey and Villabos (2007) that agroforest contains bird assemblage as abundant, species-rich and diverse as natural forest ecosystem however species structure were highly altered, with fewer forest dependent species and different dominant species. Bird diversity are more closely related to structural and floristic characteristics of every land use types. One of the important benefits provided by agroforest to biodiversity is through providing habitat for tolerant species and corridors connecting different habitats (Jose 2009). Birds plays a vital role in seed dispersal and forest recovery in agroforest ecosystems by increasing seed deposition by dispersing seeds resulting in high seedling regeneration of species not locally present in previous years (Lozada et al. 2007). According to Van Bael et al. (2007), the presence of large tress in agroforest

provides important breeding niches and food resources for many bird species and this may influence the high diversity of birds in the habitat. Almarazan-Nunez et al. (2014) found that bird abundance was higher in nature forest in the dry season and high species richness of dispersers and seed predators were positively correlated to vegetation complexity. Waltert et al. (2004) also mentioned that young secondary forest and agroforest sustain high number of bird species not significantly lower than to adjacent nearprimary forest. In agroforest, greater conservation value was found than habitats with monoculture crops. Traditional often complex agroforestry systems are more supportive than monocrop systems, however natural habitat on whose proximity may often depend for high levels of wild biodiversity are still best for many wildlife species such as birds (Mcneely & Schroth 2006; Harvey & Villalobos 2007;). Forests and agroforests replaced with simplified agricultural systems will result in shifts towards less specialized bird communities with altered proportions of functional groups (Sekecioglu 2012). Furthermore, the proximity of agroecosystem habitats to natural forest is vital for the maintenance of bird diversity and their ecological function (Tscharntke et al. 2008). Following agroforest, ricefield habitat was the second diverse habitat for birds. Similarity index between agroforest and ricefields revealed to be higher with 79.91% similarity in agroforest. Birds recorded in rice fields include wetland and migrant species such as Ardeola speciosa, Bubulcus ibis, Egretta garzetta, Lanius cristatus and Tringa stagnatilis. For birds, ricefields function as a temporary wetlands, with conditions changing drastically in the course of the year. This habitat type is essential for many bird species by providing valuable and suitable habitat for foraging and breeding activities of various kinds of bird species such as migrant birds (Tourenq et al. 2001). Seasonal changes is one of the temporal effect on habitat used by bird species (Tourenq et al. 2001) such as the Tringa stagnatilis which utilizes the rice fields during the post-harvesting season and field preparation for foraging and breeding activity. This species inhabits warm inland wetlands from open steppe to boreal forest, including shallow freshwater, grassy or marshy lake-edges (Kennedy et al. 2000; Birdlife International 2003). T. stagnatilis were found in flock feeding on many injurious pests in the paddy of ricefields. It further suggest that postharvesting season and field preparation can result to an important surges of prey availability which serves as food for birds. Wetland birds according to Comin et al. (2001) prefers a wetland with intermediate plant cover for resting and sleeping activities better than ricefields and either very open wetlands or very dense

ones with tall vegetation. However, ricefields plays an important role by mitigating the impact of wetland modification in many bird species utilizing the habitat however no legal protection for this habitat type was proposed (Sanchez-Guzman et al. 2007), also ricefields serves as a refuge for wetland birds during dry years when marshes and other wetlands are dry (Tourenq et al. 2001). Farming strategies and activities in ricefields may also affect and is important for the presence and diversity of wetland bird species (Tourenq et al. 2001). Wood et al. (2010) stated that traditional practice, with one crop each year and long periods of fallow flooding may be beneficial to many important species. In contrast with modern intensive farming with multiple cropping season and high chemical use that may implicate biodiversity decline. Moreover, flooded fields apparently provide equivalent foraging habitat to seminatural wetland and the reduced predation making it a safer habitat for many wetland bird species. Therefore, if ricefields will be managed properly it can be a valuable agricultural habitat for many wetland birds (Elphick 2000). For migrant species such as E. garzetta, A. bacchus, and B. ibis, ricefields are important feeding areas and stop-over and wintering sites (Acosta et al. 2001). To further determine the structure of bird community in relation to habitat types modification, roads and heavily disturbed habitat was assessed. Lowest species diversity was determined from this habitat type with 51% similarity between the agroforest and ricefields. The increasing prevalence of roads is one of the potential contributor to the worldwide decline of bird population (Kociolek et al. 2011). The study of Palamino and Carrascal (2007) revealed that nearby urban sites do not affect the total bird species richness in natural habitats which conforms the result of this study however bird abundance increases with reduction of distance to the nearest urban development. Studies on bird diversity in city and urbanized landscape revealed a significant impact on bird species richness and relative abundance (Gatesire et al. 2014), an increasing diversity from most to least urbanized areas was also observed from previous studies (Clegeau et al. 1998). Road density was also found to influence bird community (Minor and Urban 2009). The availability of food resources in roads and urbanized habitat is an important factor that will explain the low diversity in the study site. Further, to mitigate the negative effect of urbanization, the use of native vegetation in urban sites such as roads and buildings is recommended (Mills et al. 1989), Edge effects might be partially mitigated with vegetation management and restoration (Kociolek et al. 2011).

As a whole, commonly encountered species along the habitats were the following: Collocalia esculenta, Geopelia striata, Hirundo tahitica, Lonchura malacca, Nectarinia jugularis, Passer montanus, Pycnonotus goiavier, Rhipidura javanica, and Tachycineta bicolor. These birds are mostly associated with human communities and some are generalist feeders. Their ability and characteristics makes them easily adapted to their environment and thus they are of lower risk of extinction (Blair, 1996). Very low endemicity was noted from the agroforest with only three species (9%) were recorded as endemic in the Philippines and only two species from roads with no endemic records in ricefields. Both Phapitreron amethystina and Dicaeum australe are usually found in primary and secondary forest and also in fruiting and flowering trees from 2000 m and below elevation while Centropus viridis usually prefers grassland, mixed cultivated areas, forest and also second growth (Kennedy et al. 2000). While, majority of the species are resident species (64%) such as A. payanensis, H.tahitica, G. striata, T. bicolor and L. atricapilla. According to Paz et al. (2013) more endemic species are present in advance secondary and old growth forest. Island-endemic birds are thought to seldom use disturbed habitat such as plantation and agroforest due to their evolved morphological and behavioral characteristics resulting in their specialize preference for specific natural forest resources. But still the presence of trees in tropical land use are important for the maintenance of many resident bird species (Waltert et al. 2005) and agroforest can still support high endemic species, a study in Central Sulawesi (Abrahamczyk et al. 2008) revealed that agroecosystem particularly cacao plantation may maintain a high diverse cover of forest tress, that when managed properly, can harbor up to 60% of forest specialists and endemic birds species. In view of habitat structure, vegetation and levels of human disturbance may be an important determinants of endemic bird diversity, species richness and abundance.

Feeding Guilds Foraging habits of bird identified was assessed to explore the variation in avifaunal composition among habitat type. According to Pearman (2002), variation in vegetation structure may affects the distribution of bird foraging guild. Five feeding guilds was assessed in the study where insectivore group was the most dominant group. Insectivorous feeding guild was mostly composed of species from families Apodidae and Hirundidae such as Collocalia esculenta and Hirundo tahitica respectively. In rice fields and agroforest,

insectivore species Hirundo tahitica was recorded most abundant species. In the study, insectivore species diversity were found to be greater in agroforest compared to monoculture crop and heavily disturbed habitats such as ricefields and roads respectively. According to Blake and Loiselle (2001), insectivores are often found to be the most species rich and abundant in tropical forest types. The result of this conforms to the result of Rajashekara and Venkatesha (2014), stating that higher insectivore species was found in agroforest, and the availability of a variety of food sources for both adults and young, safe habitat for nesting and roosting in and around the agro ecosystems are important for the occurrence and abundance of insectivore species. On the hand, insectivore birds in agroforest provides benefits for farming strategies by reducing insect pet population in agricultural habitats that further enhances the conservation value of farms for birds and other wildlife species (Johnson et al. 2010). Laurance et al. (2004) further stated that in roads even without noise and traffic have greatly affected the population of insectivorous bird species which conform to the low insectivore abundance and richness found in the study site (roads). Next to insectivores, carnivorous birds were second highest group recorded particularly in ricefields. The most abundant species recorded were Egretta garzetta and Bubulcus ibis. This conforms to the report of to Munira et al. (2014) that carnivorous species such E. garzetta and B. ibis are abundant before harvest season in Northern Peninsular Malaysia. The presence of high carnivorous species in ricefields was primarily influenced by the abundance of food source such as small frogs, fish, mollusks and small vertebrate species. Stafford et al. (2010) stated that the abundance of many carnivorous bird species in ricefield may be due to large quantity of food resources such as polychaetes, crustacians and mollusks in rice plots during their migration season. Furthermore, King et al. (2010), points out that rice fields in many countries support large number of migratory waterbirds and may be an important for many species. During the rice-growing cycle, fields were most important for carnivorous birds and during the sowing stage, whereas post-harvest flooded fields were most valuable for granivorous species (Acosta et al. 2010). This conforms to the result of this study where higher granivore species richness was found in ricefields compared to other habitat types. The most abundant granivore species includes Geopelia striata, Lonchura atricapilla, Padda oryzivora, Passer montanus and Stigmatopelia chinensis. Columbids

such as G. striata and S. chinensis were commonly observed in grounds and grassy habitats were they were noted to pick grains from plant source such as rice and grasses. P. montanus is species is known to occur throughout the year in ricefields and habitats inhabited by human. L. atricapilla was once considered as National Bird of the Philippines and usually found in ricefields, grasslands and open countries usually in flock consuming grains and seeds, both species (P. montanus and L. atricapilla) were considered as pest by local rice farmers in the Philippines (Kennedy et al. 2000). Moorcroft et al. (2002) concluded that fields left fallow after harvest (i.e. stubble fields) support high wintering densities of many species of granivorous birds. Their study emphasized that variation in the abundance and availability of weed resources affect the diversity of granivorous species among habitats. Further, the presence of high diversity of granivores in a habitat indicates habitat disturbance (Gray et al. 2007). Frugivore birds were found higher in agroforest compared to ricefields. The abundance of available food resources inside the agroforest is one of the factor for the high species richness in the habitat. The abundance or richness of fruiting plants are important and associated with the diversity of frugivorous bird species and foraging behavior in a certain habitat type (Moegenburg and Levey 2003). A related findings of Blake and Loiselle (1991) that capture rate of frugivore birds in primary forest is generally were greater in periods when fruit was abundant. The presence of species belonging to the family Sturnidae, Pycnonotidae, Columbidae and Oriolidae are good indicators for forest regeneration in a semi-degraded/disturbed habitat such as agroforest. The tolerance of frugivorous species to degraded landscapes due to different land use types are important during the initial forest succession and restoration in tropical regions (Herrera 1984; Corlett 1998). Lastly, nectarivores were least recorded among habitats and no presence in ricefields. In agroforest, two species were recorded including the endemic flowerpecker Diceaum australe. The presence of nectarivore in agroforest may be explained by the availability of flowering resource in land use system and the seasonality of flower during the season. Fleming (1992) emphasized that structure and composition of avian communities change in space and time with the availability of food resources. Variation tends to be most visible among bird species that feed on patchy and temporary food resources such as nectar and fruit. Waltert et al. (2005) observed species of nectarivores in agroecosystem with decreasing diversity as the land modification increases. Cotton (2006) added that the abundance and diversity of nectarivores are correlated with increase in

nectar availability in a specific habitat. In this study, nectarivores were the least abundant and poorly documented guild, Loiselle (1988) noted that nectarivores are difficult to observe because of their small size and likely was underestimated relative to other guilds. Furthermore, according to Li et al. (2013), higher bird species richness was found in native forest than in rubber plantations, and bird community significantly varies among two habitat types. It was also found that no strict frugivores in rubber agroforest and no granivorous in semi-deciduous monsoon forest and lower species richness of insectivores and nectarivores birds in rubber agroforest than to native forest. Consequently, this study have provided an information on the diversity and structure of birds in different land-use in lowland south central Mindanao. The study suggests that the availability of diverse food source, foraging and roosting sites for diverse bird community are essential factors to their diversity and abundance in a certain habitat types. In a similar case, Azman et al. in Malaysia (2011) concluded that conversion of forest to agriculture such as oil palm plantations or to paddy fields influenced the changes in bird diversity and variation in the distribution of avian guilds. Li et al. (2013) noted that native forest are still important habitat for bird species following their result in rubber plantation and natural where richness was higher in native than that in agroforest which exactly supports the result of this study. Furthermore, this result suggests that to conservation of native, endemic and migrant species in every land-use systems, the maintenance of important food source and habitat structure for variety of bird species must be incorporated. Moreover, deforestation in Southeast Asian region if will continue, it will increase the probability of extinction of many bird species in the region (Brooks et al. 1997).

CONCLUSION

The study on the avifaunal diversity and their foraging structure were elucidated in this study. With the respect to the result of the study, following conclusions were drawn: 1) Among all land-use types, agroforest recorded the highest avifaunal diversity, 2) Higher species similarity was determined between agroforest and ricefields than in roads and urban sites, 3) Low number endemic species was found in all land-use types, 4) Insectivorous and Frugivorous species were higher in agroforest and ricefields, 5)

Vegetation structure and availability of food resources and foraging/nesting sites are important for bird species in different land use. Studies on the effect of land-use on birds in the Philippines may be scarce and therefore to further elucidate other factors affecting bird diversity in different degraded habitat, like considering spatiotemporal factors and specific food resource availability is recommended for further studies.

ACKNOWLEDGEMENT

The researchers are very grateful for the all the experts and critics who provided their constructive comments and suggestions which further lead to the improvement of this paper. Further, a small fund imparted from the project funded by Rufford Foundation was also gratefully acknowledge to the success of this paper.

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Figure 1: Map of the study site in lowland south central Mindanao, Philippines.

Figure 2: Similarity of species composition along three habitat types in lowland south central Mindanao, Philippines.

Figure 3: Abundance of birds in terms of feeding guild in different land-use type in lowland south Central Mindanao.

Figure 4: Similarity of feeding guilds on different land-use types.

Table 1: Bird species recorded from three land-use types in lowland south central Mindanao, Philippines (2014). Family

Species Name

Endemicity

Status

Feeding Guild

Agroforest

Ricefields

Accipitridae

Haliastur indus

Resident

LC

Alcenidae

Halcyon chloris

Resident

Apodidae Ardeidae

Collocalia esculenta Ardeola speciosa

Carnivore

0

2

0

LC

Carnivore

29

20

2

Resident

LC

Insectivore

18

4

25

Migrant

LC

Carnivore

5

4

0

Bubulcus ibis Egretta garzetta

Migrant

LC

Carnivore

0

30

0

Migrant

LC

Carnivore

0

40

5

Artamidae

Artamus leucorynchus

Resident

LC

Insectivore

2

14

3

Campephagidae

Lalage nigra

1

0

Chalcophaps indica

LC

Insectivore Frugivore

12

Columbidae

Resident Resident

LC

6

0

3

Geopelia striata

Resident

LC

Granivore

37

25

8

Phapitreron amethystina

Philippine Endemic Resident

LC

5

0

2

LC

Frugivore Granivore

18

6

3

Resident

LC

Granivore

0

5

0

Stigmatopelia chinensis Streptopelia tranquebarica

Road

Corvidae

Corvus cf. macrorhynchos

Resident

LC

Carnivore

15

5

3

Cuculidae

Centropus viridis

Philippine Endemic

LC

Insectivore

2

0

1

Dicaeidae

Dicaeum australe

Philippine Endemic

LC

Nectarinivore

8

0

0

Estrildidae

Lonchura atricapilla

Resident

LC

Granivore

21

29

2

Introduced

VU LC

Granivore

17

11

3

Hirundinidae

Padda oryzivora Hirundo tahitica

58

74

21

34

30

10

Laniidae

Tachycineta bicolor Lanius cristatus

Insectivore Insectivore

23

8

9

1

2

0

Resident Resident

LC LC LC

Insectivore Insectivore

Locustellidae Meropidae

Megalurus palustris

Migrant Resident

Merops philippinus

Resident

LC

Insectivore

12

41

0

Muscicapidae

Rhipidura javanica

Resident

LC

Insectivore

22

8

8

Muscicapa sp.

Resident

LC

Insectivore

2

0

0

Nectarinia jugularis

Resident

LC

Nectarinivore

25

0

9

Oriolus chinensis

Resident

LC

Frugivore

12

0

14

Nectariniidae Oriolidae

Resident

LC

Granivore

18

30

9

Pycnonotidae

Passer montanus Pycnonotous goiavier

Resident

LC

Frugivore

64

11

3

Scolopacidae Sturnidae

Tringa stagnatilis Aplonis panayensis

Migrant

LC

Carnivore

0

9

0

Resident

LC

Frugivore

21

27

25

Turdidae

Copsychus saularis

Resident

LC

Insectivore

5

0

2

Cisticolidae Abundance

Cisticola juncidis 1114

Resident

LC

Insectivore

0 492

16 452

0 170

27

25

22

Passeridae

Species Richness

33