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FOREST FRAGMENTS MATTER: A LOOK INTO THE SPECIES RICHNESS AND DIVERSITY PATTERNS OF BIRDS IN A SMALL, ISOLATED, PROTECTED LANDSCAPE IN MINDANAO ISLAND, PHILIPPINES
Renz Angelo J. Duco1* , Simeon Gabriel F. Bejar1 , Justin G. Banez2 , Jay S. Fidelino1 , Melizar V. Duya1 , Perry S. Ong1 , Mariano Roy M. Duya1
1 University of the Philippines Diliman, Philippines *e-mail: rjduco@up.edu.ph 2University of the Philippines-Philippine General Hospital, Philippines
Received: 11.12.2023. Revised: 12.04.2024. Accepted: 22.04.2024.
The establishment of Protected Areas is deemed of critical importance in global conservation initiatives, particularly in biodiverse regions and global biodiversity hotspots, such as the Philippines. However, the crucial role played by smaller Protected Areas in biodiversity conservation is frequently overlooked, making this a particular area of research interest. The Initao-Libertad Protected Landscape and Seascape (hereinafter - ILPLS) is one of the last remaining karst forests with natural vegetation and refuge for wildlife conservation on the island of Mindanao, the Philippines. However, the landscape component of this Protected Area is very small (ca. 506 000 m2), bisected by a road, and heavily disturbed by illegal logging and frequent tourist visits. From 2014 to 2018, we assessed the community structure and revealed patterns of bird diversity in ILPLS. We recorded a total of 814 individuals of birds from 36 species and nine feeding guilds from a total sampling effort of 558 230.40 mist-net hours in the Protected Areas' two management zones, namely the Special Protection Zone (SPZ) and Tourism Zone (TZ). ILPLS has a high level of endemism at 33% (12 species), including nine Philippine endemics and three Mindanao Island endemics. We also recorded Gorsachius goisagi, a globally threatened species categorised by IUCN as Vulnerable. Species richness was higher in the SPZ than in the TZ (p = 0.012), whereas no significant differences were observed in the Shannon index values (p = 0.101) and mean capture rates (p = 0.378) between the two management zones. Species and feeding guild assemblages did not differ between the two management zones (p = 0.939) but varied between vertical strata (p = 0.001). Here, we show how this small, protected landscape harbours a comparatively diverse bird community, including restricted-range species and species with high conservation priority. This suggests that forest fragments, even of this size, are important habitats for bird conservation efforts and should not be undervalued. We recommend extending such studies to other fragments, especially those that are still not protected, to improve our biodiversity database, further our understanding of biodiversity and fragment dynamics, and make a case for the protection of other forest fragment habitats.
Key words: avifauna, feeding guild, management zone, mist net, vertical stratification
Introduction
The establishment and proper management of Protected Areas are crucial measures for the conservation and restoration of habitats and native species (Pringle, 2017; Gillespie, 2020; Chowdhury et al., 2023). The rapid expansion of the global network of Protected Areas is expected to contribute to the protection and persistence of biodiversity and safeguard species with high conservation priorities (Geldmann et al., 2013; UNEP-WCMC & IUCN, 2016). However, the important role played by smaller Protected Areas in biodiversity conservation is often overlooked, making it a particular area of research interest (Baldwin & Fouch, 2018). Compared with large-sized Protected Areas, smaller-sized Protected Areas usually harbour fewer species that are predisposed to exacerbated threats from land-use change and ecological isolation (Hansen & DeFries, 2007;
Duran et al., 2016; Baldwin & Fouch, 2018). Nonetheless, these areas remain invaluable in terms of preserving biodiversity and maintaining critical ecosystem services, and thus should be given equal attention and recognition in conservation efforts (Bodin et al., 2006; Eigenbrod et al., 2009; Wintle et al., 2019).
The Philippines stands as one of the megadiverse countries; it supports a wide range of flora and fauna with high endemicity (Mittermeier et al., 1997; Fernando et al., 2008; Mohagan et al., 2015). To address significant threats to its biodiversity, the government has established a network of 248 Protected Areas, covering about 25% (78 000 km2) of the Philippines' total land area (DENR-BMB, 2022). However, half of these Protected Areas are relatively small (less than the median of 30 km2) and remain largely unexplored. One example is the Initao-Libertad Protected Landscape and Seascape (hereinafter - ILPLS), a Protected
Area with a landscape component of ca. 506 000 m2. Previous terrestrial biodiversity studies conducted within the ILPLS have primarily focused on plants (Canencia & Daba, 2015; Galindon et al., 2018) and invertebrates (Manting et al., 2013; Madjos & Demayo, 2017; Sacay & Aspe, 2023), with only one study focusing on vertebrates (Bejar et al., 2020). Furthermore, this small Protected Area is isolated into two fragments by a national road and bordered by agricultural lands and is thus susceptible to a wide range of edge effects and anthropogenic threats. Consequently, there remain significant gaps in understanding how to effectively manage such Protected Areas and similar landscapes across the Philippines, which poses challenges to the overall conservation of its biodiversity.
In this study, we aimed to evaluate the importance of ILPLS in terms of biodiversity conservation, particularly through the lens of avian diversity. Birds are often the focus of biodiversity and ecosystem studies, due to their better visibility compared to other taxa and their high sensitivity to environmental changes, which make them ideal bioindicators of ecosystem health (Chowfin & Leslie, 2021; Santangeli et al., 2023; Dela Cruz et al., 2023; Maznikova et al., 2024). Even subtle declines in the populations of common species can signal significant declines in ecosystem health (Winfree et al., 2015). Birds also play pivotal roles in supporting ecosystem health through essential ecological functions, such as seed dispersal, polli-
nation, and pest population control, and through their contributions to maintaining ecological balance and biodiversity, especially in tropical ecosystems, which constitute important ecosystem services (§ekercioglu et al., 2016; Díaz-Siefer et al., 2022). In the Philippines, birds represent the most diverse group of terrestrial vertebrates, comprising 735 species, of which 247 are exclusive to the archipelago (WBCP, 2023).
Here, we aimed to assess the bird diversity within the ILPLS based on mist-netting over a five-year period. Specifically, we identified their endemicity, residence, and conservation status based on existing listings, characterised the avian communities within the management zones of the ILPLS in terms of species and feeding guilds through standard diversity indices, and compared the vertical distribution of the bird communities across the forest's vertical strata.
Material and Methods
Study area
The Initao-Libertad Protected Landscape and Seascape (ILPLS) (8.543366° N, 124.321320° E, 40 m a.s.l.) is located at the northern Mindanao Island in the province of Misamis Oriental. The protected landscape component has a total area of 506 000 m2 and is intersected by a national highway. This division results in two management zones, namely a 360 000-m2 Special Protection Zone (SPZ) and a 140 000-m2 Tourism Zone (TZ) (Fig. 1).
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Fig. 1. Location of mist-net stations (yellow circles) within the two management zones (Special Protection zone (SPZ) and Tourism zone (TZ)) of Initao-Libertad Protected Landscape and Seascape (ILPLS) in Mindanao Island, Philippines.
Natural forest vegetation dominates the study area, including at least 15-m high native canopy tree species such as Ardisia tomentosa C.Presl, Ficus var-iegata Blume, and Pterocarpus indicus Willd., and a few exotic species such as Swietenia macrophylla King and Gmelina arborea Roxb. ex Sm., which are present in the TZ. The general vegetation is comprised of secondary growth forests over limestone.
Mist-netting
Mist-netting was performed from 2014 to 2018, covering both the wet and dry seasons, following standardised mist-net protocols (MacArthur & MacArthur, 1974). A total of 25 nylon mist nets (12.0 x 2.6 m, with a 36-mm mesh) were used, 20 of which were set near the ground level, and five nets were placed at sub-canopy (10-15 m) following the method by Ingle (1993). Nets were opened for 12 h. (06:00-18:00) for three consecutive days at each sampling point. The nets were checked every 30 min. to retrieve any captures. Field sampling and collection was covered by the Department of Environment and Natural Resources (DENR) Wildlife Gratuitous permits R10 2014-36 and R10 2018-07.
Birds were identified following Kennedy et al. (2000) and were further classified into feeding guilds based on their known food preferences (insectivores, frugivores, nectarivores, carnivores, or a combination of these) and their foraging layer (terrestrial, understory, arboreal) (Duco et al., 2021; Pabico et al., 2021). Prior to release, all captures were measured and tagged with uniquely numbered aluminum bird rings.
Data analysis
Estimated species richness was calculated using the mean of four selected non-parametric species richness estimators (Chao, Jack1, Jack2, and Bootstrap) and was compared between the two management zones and vertical strata using Community Ecology package («vegan», ver. 2.4-1) (Oksanen et al., 2020) in the R statistical software (ver. 4.1.2) (R Core Team, 2021). Sampling completeness was assessed by comparing the actual number of species sampled with the total estimated species richness, with a value higher than 90% considered sufficient (Mohd-Azlan et al., 2019). Species accumulation curves with 95% confidence intervals were also generated based on the expected species richness.
Bird diversity was estimated using Shannon's species diversity index (H'), which was computed by analysing the yearly data individually rather than pooling the data across years. Diversity be-
tween the two management zones and vertical strata was compared using the Mann-Whitney U test. This was also used to assess differences in the abundance and capture rates of birds and feeding guilds, between the two management zones and vertical strata. Capture rates were expressed as the number of individuals captured per mist-net hour. Similarity Percentage (SIMPER) test was also used to identify the species or guilds that contributed the most to the observed dissimilarities. Mann-Whitney U test was performed using IBM SPSS Statistics for Windows (ver. 20.0; IBM Corp., USA), while SIMPER was performed using PRIMER (ver. 6.4.7) (Clarke & Gorley, 2006).
Mantel test was performed to examine spatial autocorrelation in the data, with ecological matrices calculated using the Bray-Curtis dissimilarity index, a geographical distance matrix derived from Euclidean distances, and the number of permutations set at 999 based on Spearman rank coefficients. Per-mutational multivariate analysis of variance (PER-MANOVA) was used to compare species and feeding guild assemblage between the two management zones and forest vertical strata. In addition, nonmet-ric multidimensional scaling (NMDS) was used to construct two-dimensional ordination plots and visualise the results of PERMANOVA. Mantel test, PERMANOVA, and NMDS were performed using the «vegan» package (Oksanen et al., 2020) in the R statistical software (ver. 4.1.2) (R Core Team, 2021).
Results
Bird community in the ILPLS
A total of 814 individuals representing 36 species were captured from a collective sampling effort of 558 230.40 mist-net hours (Appendix 1). Most of the species (32 species) were recorded in SPZ, 15 of which were not recorded in the TZ. Meanwhile, 21 species were recorded in the TZ, with four species recorded exclusively in this zone. Most of the species captured were insectivores, namely, terrestrial insectivores (eight species), un-derstory insectivores (six species), and arboreal insectivores (three species).
Twelve (12) recorded species were Philippine endemic, including three species (Macronus striaticeps Sharpe, 1877, Phapitreron breviros-tris Tweeddale, 1877, and Phylloscopus olivaceus Moseley, 1891) that are endemic to the Mindanao faunal region. Our survey also yielded a record of Gorsachius goisagi Temminck, 1836, a threatened migratory bird species categorised as Vulnerable on the IUCN (2023) Red List.
Diversity parameters and bird composition between the two management zones in the ILPLS
Species richness was significantly higher in the SPZ (40.09 ± 1.45) than in the TZ (34.22 ± 4.99) based on the species richness estimators (U = 29.00, p = 0.012) (Table 1). In addition, the generated species accumulation curves also showed a higher number of species accumulated in SPZ compared to TZ (Fig. 2). Meanwhile, Shannon index values (SPZ: 1.82 ± 0.13; TZ: 1.49 ± 0.15) and mean capture rates (SPZ: 0.0048 ± 0.0007; TZ: 0.0036 ± 0.0006) did not differ significantly between the two management zones (SPZ: U = 143.00, p = 0.101; TZ: U = 56.00, p = 0.378). Based on PERMANOVA, bird assemblages did not differ between the SPZ and TZ (F = 0.33, p = 0.939). This is also supported by the generated NMDS plot, which showed no evident separation between samples from the two zones (Fig. 3). Instead, samples clustered together, indicating high degree of similarity in bird assemblages for the two management zones. Mantel test demonstrated the presence of spatial autocorrelation with statistically significant, albeit weak, positive correlation between the bird community composition and geographic matrices (r = 0.204, p = 0.042).
Bird feeding guild structure in the ILPLS
Nine (9) feeding guilds represented the bird community in the ILPLS. The terrestrial insectivore (TI) guild had the most representative species (eight species) and the most abundant, comprising approximately 32% (n = 257) of the total number of captures. To avoid skewing the results, we excluded two guilds (raptorials and understory insectivore-nectarivore), which had low sample sizes from our analysis.
No significant differences in species richness (U = 56.00, p = 0.378) and Shannon diver-
sity index (U = 51.00, p = 0.242) was observed between the two management zones. In addition, there was no significant difference in the overall capture rates (U = 70.00, p = 0.932) and guild assemblage (F = 0.142, p = 0.972) between the two zones.
Fig. 2. Species-accumulation curve based on mist-net captures of birds in the two management zones (SPZ -Special Protection zone, TZ - Tourism zone) of Initao-Libertad Protected Landscape and Seascape, Mindanao Island, Philippines. The dashed lines indicate 95% confidence intervals.
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Fig. 3. NMDS ordination based on mist-net captures of birds in Special Protection zone (SPZ) and Tourism zone (TZ) of the Initao-Libertad Protected Landscape and Seascape (ILPLS), Mindanao Island, Philippines.
Table 1. Observed and mean estimated species richness (± SE), number of captures, mean capture rates (± SE), diversity index (± SE), total sampling effort, and sampling completeness based on mist-netting of birds in the two management zones in the Initao-Libertad Protected Landscape and Seascape (ILPLS), Mindanao Island, Philippines
Diversity parameters SPZ TZ Total
Number of species observed 32 21 36
Mean estimated species richness ± SE 40.09 i 1.45 34.22 i 4.99 46.77 i 1.97
Number of individuals 546 268 814
Mean capture rate (capture/mist-net hour) ± SE 0.0048 i 0.0007 0.0036 i 0.0006 0.0042 i 0.0005
Shannon-Wiener index (H') ± SE 1.82 i 0.13 1.49 i 0.15 1.65 i 0.10
Total sampling effort (mist-net hours) 344 822.4 213 408 558 230.4
Sampling completeness (%) 79.83 61.37 76.97
Note: SPZ - Special Protection zone, TZ - Tourism zone.
Vertical stratification of birds in the ILPLS
Based on PERMANOVA, significant differences in bird assemblages between understory and sub-canopy across the two management zones were observed for both species assemblages (F = 19.586, p = 0.001) and feeding guilds (F = 28.687, p = 0.001). The generated NMDS ordinations also supported these results, showing a clear separation between understory and sub-canopy samples (Fig. 4).
Based on SIMPER analysis, 12 species contributed 92.09% to the observed dissimilarity between the two strata. Of these, two species (Aplo-nis panayensis Scopoli, 1786 and Phapitreron brevirostris) were significantly more abundant in the sub-canopy (U = 21.00, p = 0.002 and U = 78.00, p < 0.001, respectively), while seven
species had significantly higher capture rate in the lower forest stratum (Fig. 5). Similarly, arboreal feeding guilds (arboreal frugivore and arboreal frugivore-insectivore) showed significantly higher capture rates in the sub-canopy while terrestrial and understory guilds (terrestrial frugivore, terrestrial insectivore, understory insectivore, and understory insectivore-carnivore) had higher capture rates in the lower stratum (Fig. 6).
Both species and feeding guild richness were also significantly higher in the understory than in the sub-canopy layers (U = 33.00, p = 0.024; U = 32.50, p = 0.020, respectively) (Fig. 7). Meanwhile, the Shannon diversity index was significantly higher in the lower strata for species (U = 12.00, p < 0.001) but not for feeding guilds (U = 56.00, p = 0.378).
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Fig. 4. NMDS ordination of understory and sub-canopy samples of (a) species assemblages and (b) feeding guilds of birds in the Initao-Libertad Protected Landscape and Seascape, Mindanao Island, Philippines.
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Fig. 5. The mean capture rate of species that contributed to the differences in assemblage between the two forest strata of the Initao-Libertad Protected Landscape and Seascape on Mindanao Island, Philippines. Asterisks indicate significant differences based on Mann-Whitney U test: ** - p < 0.01, *** - p < 0.001.
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Fig. 6. Comparison of mean capture rate of feeding guilds between understory and sub-canopy in the Initao-Libertad Protected Landscape and Seascape, Mindanao Island, Philippines. Asterisks indicate significant differences based on Mann-Whitney U-test (** - p < 0.01, *** - p < 0.001). Designations: AF - arboreal frugivore, AFI - arboreal frugivore-insectivore, AI -arboreal insectivore, TF - terrestrial frugivore, TI - terrestrial insectivore, UI - understory insectivore, UIC - understory insectivore-carnivore.
Discussion
Despite their considerable global prevalence, small Protected Areas are undervalued and overlooked in terms of research efforts, conservation initiatives, and financial allocations (Baldwin & Fouch, 2018; Wintle et al., 2019). It is noteworthy that more than half of the Protected Areas worldwide occupy less than 1.0 km2 in size (Deguignet et al., 2014; Armsworth et al., 2018; Capano et al., 2019). Despite this, small Protected Areas remain a valuable tool for advancing global conservation goals by improving landscape connectivity and protecting threatened and endemic species (Stolton et al., 2014; Armsworth et al., 2018).
Comparison across Protected Areas and key biodiversity areas in Mindanao Island
We have observed a relatively lower bird species richness and diversity in the ILPLS compared to some nearby Protected Areas and key biodiversity areas across Mindanao Island (BMB, 2015; Nu-neza et al., 2019; Gracia et al., 2021; Senarillos et al., 2021). This observed variation in species richness may be influenced by several factors including differences in sampling efforts and the effect of area size, altitude, and habitat heterogeneity. For instance, sampling effort was not standardised across studies
Fig. 7. Differences in estimated species richness and diversity (Shannon index) between understory and sub-canopy captures of bird species and feeding guilds in the Initao-Libertad Protected Landscape and Seascape, Mindanao Island, Philippines. Asterisks indicate significant differences based on Mann-Whitney U test (* - p < 0.05, *** - p < 0.001).
and as such, differences in diversity may be artifacts of the efforts and methods employed. Our capture effort was also insufficient to reach a plateau in the species accumulation curve, even with a long sampling duration, which suggests that our findings may have underestimated the true species richness of birds in the ILPLS. Previous surveys were also conducted in relatively larger Protected Areas, which could have a higher capacity to harbour more species. This is in accordance with the results of a recent global meta-analysis conducted by Timmers et al. (2022), which showed a general decline in bird occurrence with a decrease in forest fragment size. Finally, the study sites were also mountainous areas, and most of the surveys were conducted at different altitude gradients, a habitat feature which could attract more species because of more available microhabitats and resources (McCain & Grytnes, 2010). ILPLS, meanwhile, has a relatively smaller area and is generally located in the lowlands, and thus has a limited microhabitat and resources compared with other Protected Areas in the region. However, it is essential to note that the effect of Protected Area size and altitude in avian species richness and diversity within the above-mentioned sites was not investigated in the current study. This aspect deserves thorough exploration and comprehensive analysis in future studies.
Bird and feeding guild assemblage between the two management zones
We recorded a higher species richness in the SPZ (32 species) than in the TZ (21 species). In addition, a higher number of rare and endemic species was recorded in the SPZ compared to TZ (Appendix 1). Endemic and threatened species are known for their high sensitivity to the quality of vegetation within forest patches, showing a preference for denser patches, where vegetation is abundant and diversified to offer resources and protection (Marzluff, 2001). Since the SPZ has a relatively larger patch size compared to the TZ, SPZ is expected to support a higher number of these species because of a higher degree of habitat heterogeneity and increased availability of resources (Zanette et al., 2000; Jokimaki et al., 2005). However, bird species that are common in agricultural and disturbed areas were also observed in the SPZ. This includes Geopelia striata Linnaeus, 1766, Lanius schach Linnaeus, 1758, and Lonchura leucogastra Blyth, 1846, all of which were exclusively recorded in the SPZ. Todiramphus chloris Boddaert, 1783 and Lanius cristatus Linnaeus, 1758, both of which are known to be disturbance-tolerant species, were also significantly more abundant in the SPZ than in
the TZ. The influx of these disturbance-tolerant species in the SPZ may have been caused by apparent increased edge effects, which is characteristic of fragmented habitats (Banks-Leite et al., 2010; Hatfield et al., 2020). These disturbance-tolerant species, which are also mostly generalists, may exploit available resources at the forest edge, such as open and grassland areas, where higher foraging opportunities are present (Banks-Leite et al., 2010).
Meanwhile, the low bird richness in the TZ may be attributed to disturbances present in the area, as human-induced disturbances generally contribute to low bird species richness and abundance in tropical forests (Vijayan & Gokula, 2006; Pardini et al., 2009). The decrease in forest cover in TZ caused by the continuous development of park infrastructure, as well as the establishment of a reforestation site dominated by exotic species, such Swietenia macro-phylla and Gmelina arborea in the TZ area, may have also contributed to the lower richness and abundance of birds in the site. This is in accordance with other studies showing that a decrease in structural heterogeneity and forest cover leads to a lower abundance and richness of bird species (Paz et al., 2013; Boha-da-Murillo et al., 2020). Frequent human visitation in the TZ could also cause disturbance in the bird community, leading to a low richness and decrease in bird abundance as observed in other studies done in fragmented habitats (Fernandez-Juricic, 2004; Kang et al., 2015). Reduced availability of resources is also expected with increased human visitations in these fragments causing a decline in population for some species (Hammit & Cole, 1998; Fernandez-Juricic, 2002, 2004). Further, noise pollution and increased waste generation associated with the development of the area for tourism can have a significant impact on the density and behavioural patterns of local species (Bhardwaj et al., 2015). However, as visitors serve as a source of income for the local people and for maintenance of the Protected Area facilities, alternative strategies should be considered including the creation of buffer zones, fencing sensitive bird habitats within forest fragments to reduce the direct impacts of human activities on nesting and foraging sites, implementing guided visitations, and providing programs to educate visitors and local residents (Ikuta & Blumstein, 2003; Fernandez-Juricic, 2004; Hostetler et al., 2008).
Insectivores were the most dominant guild in the study area, both in terms of captures and species richness, which is in accordance with other studies conducted in other lowland tropical forests (Blake & Loiselle, 2001; Relox et al., 2011; Duco et al., 2021;
Pabico et al., 2021). Insectivorous birds, with their specialised foraging strata and behaviour, drastically respond to habitat complexity structures, making them particularly susceptible to habitat disturbance especially in tropical regions (Castaño-Villa et al., 2019). Considering their sensitivity to disturbance, they often become the first group to disappear in modified and fragmented habitats as they have a high habitat specificity and relatively low range and mobility compared to other species (§ekercioglu et al., 2002; Powell et al., 2015). Terrestrial insectivores were also found to respond negatively to anthropogenic disturbance, which reflects the limited ability of this group to cross open areas and move between more suitable forest habitats (Pabico et al., 2021).
There is a high species turn-over between the two management zones with only 15 and four species caught exclusively in SPZ and TZ, respectively, which suggests that the national highway does not totally isolate the bird communities between zones, unlike for other terrestrial species inhabiting the site (Bejar et al., 2020). This may also explain the spatial autocorrelation between the zones in terms of bird community assemblage. The species exclusive to each zone mainly consisted of species with fewer than five individuals (all but one species), which resulted in negligible difference in the capture rate and assemblage of birds between the two management zones. Nonetheless, the number of individuals captured for each species and feeding guild during this study were clearly fewer in TZ, which may indicate the negative effects of fragmentation and frequent anthropogenic disturbances inside the tourism zone.
Vertical stratification
Vertical stratification of assemblages in tropical forests greatly contributes to its diversity (Oliveira & Scheffers, 2019; Thiel et al., 2021). Among animal groups, birds are well studied because they provide a good illustration of stratification in the vertical layer, forming groups of species that characterise the ground, sub-canopy, and canopy layers (Pearson, 1971; Acharya & Vijayan, 2017). However, disturbance in habitat could also alter the vertical structure of the bird community (Whitworth et al., 2016; Dinanti et al., 2018). For instance, a vertical shift towards the understory may be observed for arboreal bird species in more disturbed habitats with reduced canopy cover and vertical vegetation structure (Wunderle et al., 2005; Duco et al., 2021).
In this study, a distinct pattern of vertical stratification was observed in species and feeding guild assemblages between the understory and sub-cano-
py forest strata. Moreover, the birds were situated in their preferred strata, as predicted based on their assigned feeding guilds. This means that disturbances may have little to no effect on the vertical assemblages of birds in ILPLS, which may be attributed to the retention of the complex vegetation structure in the Protected Area and the abundance and availability of resources in both forest layers (Basham et al., 2023). The heterogeneous nature of the vegetation promotes the co-occurrence of more species as it provides a higher number of niches for birds to occupy (Chamberlain et al., 2007).
Significance of ILPLS as a habitatfor threatened and endemic bird species
Despite being small and fragmented, ILPLS still harbours threatened and endemic species, which highlights its importance as a habitat for species with high conservation value and restricted range. Endemics comprise more than one-third of the total number of species recorded. The relatively intact, dense, and diverse natural vegetation and structure of ILPLS may have played a role in the richness of endemics. This is supported by previous studies that have shown a strong correlation between vegetation intactness and the structure and richness of endemic bird species in tropical forests, as these features are assumed to support a variety of bird species and their different life histories (Mills et al., 1991; Daniels et al., 1992; Mejías & Nol, 2020; Gracia et al., 2021).
Our study also recorded the presence of Gor-sachius goisagi, a threatened species assessed as Vulnerable according to IUCN (2023). Gorsachius goisagi is a migratory, forest-dwelling species. Its presence underscores the importance of ILPLS and other forested and intact areas (e.g. Protected Areas and key biodiversity areas) as refuge, resting stops and routes for threatened migratory bird species in the region (Runge et al., 2015).
Meanwhile, Phapitreron brevirostris, an endemic bird species to the Mindanao faunal region, is one of the most abundant species captured during this study. Large-bodied frugivorous birds, such as pigeons and parrots, play an important role in regeneration and rehabilitation of degraded habitats, and fragmented forests being effective seed dispersers (Corlett, 1998, 2009). However, studies have shown that large-bodied frugivores are more vulnerable to extinction after disturbance than any other taxa (Owens & Bennett, 2000; Gomes et al., 2008; Martin & Blackburn, 2010; Sodhi et al., 2010; Española et al., 2013). The abundance of Phapitreron brevirostris and the occurrence of other frugivores such as Ram-
phiculus leclancheri Bonaparte, 1855, Chalcophaps indica Linnaeus, 1758, Bolbopsittacus lunulatus Scopoli, 1786, and Loriculus philippensis Müller, 1776, suggest that ILPLS is an important area for long-term persistence of these ecologically-important and threatened species.
Protection of small fragments ensures that these areas can be effective biodiversity preserves for threatened species. A global meta-analysis done by Timmers et al. (2022) showed that small forest areas subjected to strict protection measures have a high conservation value for forest-dependent bird species.
Conclusions
Our five-year study has revealed a rich avian diversity of ILPLS, despite its relatively small area. This, along with the high rate of endemism, the presence of globally threatened and migratory species, and the presence of both forest-dwelling and migratory species, strengthens the need for the continuous protection and preservation of ILPLS. Our data suggest no apparent differences in diversity patterns and composition of birds between the two management zones, which was expected given the proximity and similarity in environmental and floristic composition between the zones. However, the lower abundance of birds captured in the tourism zone should still be of concern as this could be driven by anthropogenic pressures (i.e. human access, regular tourist visits, building construction, maintenance practices). We also observed a clear vertical stratification of bird assemblages, which could have contributed to the diversity of birds in the protected area. Maintaining a complex vegetation structure is encouraged to ensure the availability and abundance of resources to attract more bird species. Here, we show how this small protected forest fragment still harbours a comparatively diverse bird community, which suggests that forest fragments, even of this size, are still important. ILPLS is just one of the many forest patches, which is under threat from persistent forest destruction and land conversion. Hence, we recommend extending biodiversity studies to other fragments, especially those that are still not protected, to improve our biodiversity database, to further our understanding of biodiversity and forest fragment dynamics, and to make a case for the protection of other forest fragment habitats.
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Appendix 1. List of birds recorded in Initao-Libertad Protected Landscape and Seascape including their assigned feeding guilds, residence status, endemicity, conservation status based on IUCN (2023), and the number of individuals captured in the two management zones, namely Strict Protection Zone (SPZ) and Tourism Zone (TZ).
Species Guild* Residence status** Endemicity* IUCN (2G23) SPZ TZ
Accipiter soloensis Horsfield, 1821 R M - LC G 1
Accipiter virgatus Temminck, 1822 R R - LC 1 G
Anthreptes malacensis Scopoli, 1786 UIN R - LC 1 1
Anthus gustavi Swinhoe, 1863 TI M - LC 1 G
Anthus rufulus Vieillot, 1818 TI R - LC G 1
Aplonis panayensis Scopoli, 1783 AFI R - LC 38 15
Bolbopsittacus lunulatus Scopoli, 1786 AF E Philippines LC 14 2
Caprimulgus manillensis Walden, 1875 AI E Philippines LC 1 G
Chalcophaps indica Linnaeus, 1758 TF R - LC 45 2G
Cinnyris jugularis Linnaeus, 1766 UIN R - LC 2 G
Copsychus mindanensis Boddaert, 1783 TI E Philippines LC 79 2б
Dicaeum australe Hermann, 1783 AF E Philippines LC б G
Erythropitta erythrogaster Temminck, 1823 TI NE - LC 2 G
Geopelia striata Linnaeus, 1766 TF R - LC 3 G
Gorsachius goisagi Temminck, 1835 TI M - VU 1 G
Halcyon coromanda Latham, 1790 UIC M - LC б б
Hierococcyx pectoralis Cabanis & Heine, 1863 UI E Philippines LC G 1
Hypothymis azurea Boddaert, 1783 UI R - LC 5 1
Hypsipetes philippinus Forster, 1795 AFI E Philippines LC 24 12
Lalage nigra Forster, 1781 AI R - LC 1 G
Lanius cristatus Linnaeus, 1758 UI M - LC 48 19
Lanius schach Linnaeus, 1758 UI R - LC 1 G
Lonchura leucogastra Blyth, 1846 TF R - LC 1 G
Loriculus philippensis Müller, 1776 AF E Philippines LC 1 G
Macronus striaticeps Sharpe, 1877 TI E Mindanao and Eastern Visayas LC 2G 15
Merops americanus Müller, 1776 AI R - LC 4 G
Phapitreron brevirostris Tweeddale, 1877 AF E Mindanao (Greater) VU б1 5G
Phylloscopus borealis Blasius, 1858 UI M - LC G 1
Phylloscopus olivaceus Moseley, 1891 UI E Mindanao and Eastern Visayas LC 2 G
Pitta sordida Müller, 1776 TI R - LC 23 9
Poliolophus urostictus Salvadori, 1870 AFI E Philippines LC 22 14
Psilopogon haemacephalus Müller, 1776 AFI R - LC 2 G
Pycnonotus goiavier Scopoli, 1786 AFI R - LC 1 1
Ramphiculus leclancheri Bonaparte, 1855 AF NE - LC 2 1
Rhipidura nigritorquis Vigors, 1831 TI E Philippines LC 52 28
Todiramphus chloris Boddaert, 1783 UIC R - LC 7б 44
Note: Designations: SPZ - Strict Protection Zone, TZ - Tourism Zone. * - AF - arboreal frugivore, AFI - arboreal frugivore-insectivore, AI - arboreal insectivore, R- Raptorial, TF - terrestrial frugivore, TI - terrestrial insectivore, UC - understory carnivore, UI - understory insectivore, UIC - understory insectivore-carnivore, UIN - understory insectivore-nectarivore; ** - E - endemic, M - migrant, N - near-endemic, R - resident; *** - LC - Least Concern; VU - Vulnerable.
ФРАГМЕНТЫ ЛЕСА ИМЕЮТ ЗНАЧЕНИЕ: ОБЗОР ВИДОВОГО БОГАТСТВА
И РАЗНООБРАЗИЯ ПТИЦ НА НЕБОЛЬШОЙ ИЗОЛИРОВАННОЙ ОХРАНЯЕМОЙ ТЕРРИТОРИИ НА ОСТРОВЕ МИНДАНАО (ФИЛИППИНЫ)
Р. А. Ж. Дуко1'* , С. Г. Ф. Беджар1 , Дж. Г. Баньес2 , Дж. С. Фиделино1 , М. В. Дуйя1 , П. С. Онг1 , М. Р. М. Дуйя1
1Университет Филиппин Дилиман, Филиппины *e-mail: rjduco@up.edu.ph 2Университет Филиппин - Филиппинская больница общего профиля, Филиппины
Учреждение особо охраняемых природных территорий (ООПТ) считается критически важным в глобальных природоохранных инициативах, особенно в глобальных горячих точках биоразнообразия, таких как Филиппины. Однако решающая роль, которую играют небольшие ООПТ в сохранении биоразнообразия, часто упускается из виду, что повышает интерес к этой области исследований. ООПТ Инитао-Либертад - один из последних сохранившихся карстовых лесов с естественной растительностью и убежище для сохранения дикой природы на острове Минданао, Филиппины. Однако территория суши этой ООПТ очень мала (около 506 000 м2). Она разделена дорогой и сильно нарушена незаконными вырубками и частыми посещениями туристов. В 2014-2018 гг. была проведена оценка структуры сообщества птиц и выявлены закономерности разнообразия птиц на ООПТ Инитао-Либертад. За 558 230.40 ч. отлова паутинной сетью в двух зонах ООПТ (зона особого режима охраны (ЗОРО) и зона туризма (ТЗ)) в общей сложности было зарегистрировано 814 особей птиц 36 видов, относящихся к девяти трофическим группам. ООПТ Инитао-Либертад имеет высокий (33%, 12 видов) уровень эндемизма, включая девять эндемиков Филиппин и три эндемика острова Минданао. Был также отмечен угрожаемый вид Gorsachius goisagi, отнесенный МСОП к категории уязвимых (VU). Видовое богатство в ЗОРО было выше, чем в ТЗ (p = 0.012), тогда как существенных различий в значениях индекса Шеннона (p = 0.101) и средних значениях коэффициента отлова (p = 0.378) между двумя зонами не обнаружено. Видовой состав и трофические группы не имели значимых различий между зонами ООПТ, ЗОРО и ТЗ (p = 0.939), но значимо различались между ярусами леса (p = 0.001). Таким образом, было показано, что на этой небольшой ООПТ обитает сравнительно разнообразное сообщество птиц, включая виды с ограниченным ареалом и виды с высоким природоохранным статусом. Это свидетельствует о том, что даже такого незначительного размера фрагменты леса являются важной средой обитания для усилий по сохранению птиц, и их не следует недооценивать. Рекомендовано расширить такие исследования на другие фрагменты природных территорий, особенно на те, которые до сих пор не охраняются, чтобы улучшить наши знания о биоразнообразии, углубить понимание динамики биоразнообразия и фрагментов, а также обосновать необходимость защиты других фрагментов лесов.
Ключевые слова: вертикальное распределение, зона управления, орнитофауна, паутинная сеть, трофическая группа
