DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO

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1 Malays. Appl. Biol. (2018) 47(1): DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO PANG SING TYAN 1*, ATTIQQAH FADZILIAH SAPIAN 1, KHATIJAH ISMAIL 1, KOK CZE JHIN 2 and ANDREW ALEK TUEN 1 1 Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak 2 Faculty of Resource Science and Technology, Universiti Malaysia Sarawak * tyanpang@gmail.com Accepted 8 March 2018, Published online 31 March 2018 ABSTRACT Studies on wildlife food resources are important, providing insights into why certain species are abundant while others are not. This is based on the premise that wildlife are attracted to a particular habitat due to abundance of food resources. Small passerine birds inhabit different habitat types in Borneo, but the contribution of diet to this success is seldom investigated. This study aims to determine the diet of the passerine birds in six different habitat types, agro-, secondary, logged, primary, limestone forest and oil palm plantation. 253 individuals from 34 species of passerine birds were captured. Sources for dietary analyses comprised 149 regurgitated, 85 faecal and 33 stomach content samples, which were subsequently examined for prey items. Fifteen orders of prey items were identified, of which 14, 11, 8, 7, 6 and 3 were associated with agro-, secondary, logged, primary, limestone forest and oil palm plantation, respectively. Coleoptera were found eaten by 40% of the birds, followed by Hymenoptera (25%), Arachnidae (9.7%) and Orthoptera (7.5%). Regurgitated samples yielded 15 individuals of intact prey items whereby stomach content and faecal sample had one each. This study showed that Coleoptera are important food for small passerine birds inhabiting different habitats in Sarawak, Borneo. Key words: Passerine birds, diet, agroforest, secondary forest, logged forest, primary forest, limestone forest, oil palm plantation INTRODUCTION Bornean avifauna community is made up of 674 species from 20 orders (Lepage, 2017). Passeriformes, with 298 species, is the largest order of Bornean birds. They occupy a wide range of habitats that vary in altitude and disturbance level, from undisturbed montane forests, to heavily disturbed lowland forests, urbanised area or plantation (Myers, 2009; Zakaria & Rajpar, 2010; Achondo et al., 2011; Phillipps & Phillipps, 2014). Their occupation of this wide range of habitat is probably associated with the availability of food resources. Thus, dietary studies can provide clues to their resilience and success. In the lowlands, the existence of different habitats are due to anthropogenic activities (Barlow et al., 2006). For example, logged-over forest due to logging, secondary forest resulting from shifting cultivation and oil palm plantation established by private companies and government agencies. These different habitats offer different resources to the resident population of avifauna. Monotypic habitats, such as oil palm plantations, may offer less resources compared to habitats which are more complex, such as primary forests. The diet of birds has been studied via observations on foraging (Mohd-Azlan et al., 2014; Mansor et al., 2015; Styring et al., 2016), inspection of the faecal samples (Ralph et al., 1985; Chaves & Alves, 2013), analysis of the stomach contents (Ballarini et al., 2013; Amit et al., 2015), stomach flushing (Moorman et al., 2007; Fijn et al., 2012) and examination of regurgitated samples (Poulin et al., 1994; Sherry et al., 2016). Observational techniques are more appropriate for large-bodied water birds as they are easier to detect in open space habitats (Liordos, 2010), but difficult to be detected in the forest due to their often small body size, and amongst thick foliage (Blake & Loiselle, 2001; Zakaria & Rajpar, 2010). * To whom correspondence should be addressed.

2 240 DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO Despite the large number of studies on diets of birds, few have addressed passerine birds diets in Borneo (Yong, 2009). The aim of this study was to determine the diet of passerine birds in various habitats in Sarawak. MATERIALS AND METHODS Study sites The sampling took place at 22 sites across Sarawak, extending from Bau district in the west, to the central part, encompassing Kapit division, and extending north to Baram. Of these, eight were agroforests, eight secondary forests, three loggedover forests, and one each were primary dipterocarp forest, limestone forest, and oil palm plantation. Figure 1 shows location of each area, and indicate their respective forest type. Field sampling Discontinuous sampling using mist nets (9 m long, 2.5 m high with 3 shelves and 20 mm mesh size) were used to capture passerine birds from December 2014 until May Net-checking was done at two hours interval daily from dawn (0600 hour) to dusk (1800 hour) and any birds caught in the net were removed carefully and kept in a cloth bag prior to being measured, weighed, ringed and released. All birds were identified using Myers (2009) and Phillipps and Phillipps (2014). Three types of dietary samples were collected: regurgitated material, faecal samples and stomach content samples. Regurgitated samples were collected by administrating birds with 1 ml of 1.5% tartar emetic solution (prepared by diluting 7.5 g antimony potassium tartrate (APT) in 500 ml of distilled water) per 100 g bird body weight (Sing- Tyan et al., 2017). Each bird was then gently put into a cylindrical collection chamber with holes for ventilation and the chamber with bird was covered with cloth to allow it to calm down. Birds were released ten minutes later, irrespective of whether they had regurgitated or not. In this study, the ATP solution was only administered to the passerine birds caught in between 1000 to 1800 hour. By following this schedule, the birds have the opportunity to digest food taken in the early morning or to keep food foraged late in the afternoon in their stomachs for the night. Commercial glucose solution was given to some birds that showed sign of weakness after the regurgitation had taken place, to regain their strength prior to release. The collection of faecal matter (following Ralph et al., 1985; Parrish et al., 1994; Burger et al., 1999) was relatively simpler. Nevertheless, getting this was by chance during the placement of birds in the cloth-bags after they were removed from the net, and often, none. Occasionally, birds defecated during the retaining after ATP solution was given, some of them excreted instead of regurgitated in the chamber. The stomach content samples were collected from the individual birds that died accidentally. Majority of accidental death occurred in birds that remained very weak even after given commercial glucose solution. Identification of prey items All samples were put in a vial containing 75% ethanol for preservation and labelled with the species name, date, time and location of capture, and brought back to laboratory for identification under a microscope. All prey items in the samples that were preserved in ethanol were examined using a binocular stereoscopic microscope (Motic, BA410 Fig. 1. The location of the three main sampling area and each locality with the respective forest type.

3 DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO 241 Fig. 2. Intact body of an ant (Hymenoptera) found in the stomach of a Black-throated Babbler. Fig. 3. Intact body of a caterpillar retrieved from regurgitated sample of Fluffy-backed Tit Babbler. Fig. 4. Intact body of a weevil (Coleoptera) obtained from Horsfield s Babbler. Fig. 5. Intact body of a bee (Hymenoptera) extracted from faecal sample. series, China) at magnifications of 10. Prey items were examined for both intact body or fragmented body parts and identified to the lowest level of classification, mostly at the ordinal level, by referring to Capinera (2010) and Hill and Abang (2010). Most prey items in the sample were greatly fragmented, making it difficult to count individual prey items consumed by each bird. Therefore, the number of samples that contained identifiable prey items were recorded and analysed using Chi-square test. RESULTS A total of 267 samples, comprising 33 (13%) stomach contents, 85 (32%) faecal samples and 149 (55%) regurgitation samples were collected and analysed in the laboratory (Table 1). The samples were collected from 253 individuals representing 34 passerine bird species, which mainly made up of insectivores such as babblers (16 sp.), and flycatchers (six sp.). Seventeen intact prey items were identified, 15 from regurgitated samples, and one each from faecal sample and stomach content. Table 2 shows the list of prey items intact body and species of birds that consumed them. Majority of prey items consumed by passerine birds were arthropods, represented by 14 orders, compared to gastropod with only one species recorded unexpectedly in one individual (Figure 6). As the numbers of individual prey items were hard to estimate due to high degree of fragmentation, the following percentages of prey items in the bird diet were based on the number of birds found consuming the items. Chi-square test showed that the number of birds consuming different prey items were significantly different (p<0.01). Coleopterans was found in 40% of the birds, followed by Hymenopterans, Arachnids and Orthopterans with

4 242 DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO Table 1. The list of passerine birds and type of samples collected from them No. Bird species R F S 1 Black-and-red Broadbill Rufous-winged Philentoma Pied Fantail Crested Jay Black-naped Monarch Indian Paradise-flycatcher Rufous-tailed Tailorbird Hairy-backed Bulbul Grey-cheeked Bulbul Red-eyed Bulbul Spectacled Bulbul Chestnut-backed Scimitar Babbler Black-throated Babbler Chestnut-rumped Babbler Grey-headed Babbler Striped Tit Babbler Fluffy-backed Tit Babbler Chestnut-winged Babbler Sooty-capped Babbler Scaly-crowned Babbler Rufous-crowned Babbler Moustached Babbler Black-capped Babbler Short-tailed Babbler Ferruginous Babbler White-chested Babbler Horsfield s Babbler Bornean Blue Flycatcher Malaysian Blue Flycatcher White-tailed Blue Flycatcher Grey-chested Jungle Flycatcher Brown-chested Jungle Flycatcher Pygmy Blue Flycatcher Yellow-bellied Prinia R = Regurgitated sample F = Faecal sample S = Stomach content Table 2. List of intact prey items found, in accordance to sample types and bird species No. Species Sample type Prey item Figure 1 Black-capped Babbler R Coleoptera 2 Black-naped Monarch R Odonata 3 Black-throated Babbler R Hymenoptera-2 sp. 4 Black-throated Babbler S Hymenoptera 2 5 Bornean Blue Flycatcher R Lepidoptera 6 Chestnut-winged Babbler R Hymenoptera, Acarina 7 Chestnut-winged Babbler R Hymenoptera 8 Fluffy-backed Tit Babbler R Hymenoptera 9 Fluffy-backed Tit Babbler R Caterpillar 3 10 Fluffy-backed Tit Babbler R Phasmida 11 Horsfield s Babbler R Coleoptera 4 12 Moustached Babbler R Diptera 13 Short-tailed Babbler F Hymenoptera 5 14 Short-tailed Babbler R Hymenoptera 15 White-chested Babbler R Diptera

5 DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO 243 Fig. 6. Composition of prey items found from the passerine birds caught in the study. Table 3. Total number of birds containing prey according to habitat types with prey items found Order Agroforest Limestone Logged Oil Palm Primary Secondary forest forest Estate forest forest 1 Acarina Arachnidae Caterpillar Coleoptera Dictyoptera Diptera Ephemeroptera Hemiptera Hymenoptera Isoptera Lepidoptera Odonata Orthoptera Phasmida Gastropods Total Number of prey orders %, 9% and 7% respectively. Prey items that were found in low frequency were the Ephemeropterans, Lepidopterans, Phasmids and Gastropod. Coleoptera and Arachnidae were found in birds that were caught in all forest types. Orthoptera and Diptera were also found in birds from all habitat types, except oil palm plantation. The least-often encountered orders; Ephemeroptera and Lepidoptera were consumed by birds in agroforests, while Gastropods were consumed by a bird from a logged forest (Table 3). Agroforests had the highest number of birds with prey items, followed by secondary forest, logged forest, primary forest, limestone forest, and lastly oil palm estate, in decreasing order. DISCUSSION Despite intact bodies of prey being found occasionally in faecal samples (Ralph et al., 1985) and stomach content (Amit et al., 2015), they generally contain more fragmented sample than

6 244 DIET OF PASSERINE BIRDS FROM DIFFERENT HABITAT TYPES IN SARAWAK, BORNEO regurgitated sample (Moorman et al., 2007; Capinera, 2010). The findings in this study reported that 8% of regurgitated samples found were intact bodies, whereby only 3% and 1% of stomach contents and faecal sample were found containing intact samples, respectively. Like many other studies on avian diet, the diets of the passerine birds in this study were dominated by the Coleopterans. Coleopterans are known to be the largest group of insect worldwide (Hill & Abang, 2010). Body sizes vary from minute (length 0.5 mm) to large (150 mm) which make them ideal food for the passerine birds in terms of size and availability. Though winged, many of Coleopterans move relatively slowly and crawl on the forest floor. This make them an easy target for many insectivores. On the other hand, the frequent discovery of Coleopterans in the diets could also be due to their sclerotized hard elytra that are more resistant to digestion compared to other insects. The second most common prey items found was the Hymenoptera, comprising mainly of ants, while the Arachnida (spiders and scorpions) was the third most common prey item in this study, both orders found mainly on the forest floor. This is because the babblers being the predominant passerine birds found in this study generally forage on grounddwelling arthropods on the forest floor (Mansor et al., 2015). Other prey items that are found on the forest floor include gastropod which was recorded from the stomach content of one Fluffy-backed Tit Babbler. Data in Table 3 suggested that fewer birds containing fewer prey items were recorded from oil palm and limestone forest, and in primary forest compared to secondary and agroforests. While this may be an artefact of unequal sampling effort (only one site each for oil palm and limestone, two sites for primary forest compared to seven sites for agroforest and secondary forest), there is no denying that oil palm plantations are generally depauperate compared to forest (Tuen et al., 2016). Bruhl and Eltz (2010) and Fayle et al. (2010) reported huge reduction of ant diversity in oil palm plantations compared to forests. Coleopterans and Arachnids were found in the diets of birds captured in all habitats with the highest record in agroforest and secondary forest; both habitats were represented by seven sampling sites. As the disturbed habitats such as agroforest and secondary forest also harbour highly adaptive wildlife (Peh et al., 2005, 2006; Edwards et al., 2011; Edwards et al., 2014; Hamer et al., 2015) such as babblers and bulbuls in this study, foods for these birds could be supplied sufficiently in these habitats compared to others. Moreover, growing plants in agroforest and secondary forest that associate closely with insects could have attracted many insectivorous birds there. Low yield on diet sample from logged forest, limestone forest, primary forest and oil palm plantation could have resulted from less effort used during sampling in the said habitats because previous study reported that Yellow-vented Bulbul, dominant bird species in oil palm found that they fed on groups of insects of the order Coleoptera, Hemiptera, Diptera and Hymenoptera but avoided Odonata, Orthroptera, Dictyoptera and Lepidoptera (Amit et al., 2015). What is obvious from Table 3 was that the diet breath of birds in oil palm was reduced compared to limestone forest although both habitat types were represented by one sampling site. CONCLUSION This study shows that, while faeces or stomach content can yield valuable information on the diet of passerine birds, regurgitation samples have an added advantage of yielding more intact samples which then permit a more accurate assessment of the number of prey consumed by each individual. Ground-dwelling arthropods were found to be the dominant food resource consumed by most passerine birds captured in this study. Of all orders, Coleoptera and Arachnidae were recorded in all habitat types, which make them an important food resource for passerine birds in Borneo. ACKNOWLEDGEMENTS Special thanks go to Sarawak Energy (E14051/ GL(I01)/51/SEB/2014/01(02)) and Malaysian Palm Oil Board (E14051/(I01)/51/MPOB/04/2016) for research grants, and Forest Department Sarawak for a research permit (NCCD (Jld. 10)-131). Deepest gratitude is expressed to Mr. Isa Sait, Mr. Mohd. Hasri Al-Hafiz Haba and Miss Rahah Mohd. Yakup for their endless assistance and guidance throughout this study. 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