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Forest Ecology and Management 261 (2011) 531–544

Contents lists available at ScienceDirect

Forest Ecology and Management

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Bird community assembly in Bornean industrial tree plantations:Effects of forest age and structure

Alison R. Styringa,1, Roslina Ragaib,2, Joanes Unggangb,2, Robert Stuebingb,3,Peter A. Hosnerc,4, Frederick H. Sheldonc,∗

a The Evergreen State College, Olympia, WA 98505, United Statesb Grand Perfect Sdn. Bhd., ParkCity Commerce Square, 97000 Bintulu, Sarawak, Malaysiac Museum of Natural Science, Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, United States

a r t i c l e i n f o

Article history:Received 24 June 2010Received in revised form 1 November 2010Accepted 2 November 2010Available online 30 November 2010

Key words:Acacia mangiumChronosequenceLogged forestMangiumSabahSarawakSuccession

a b s t r a c t

Plantations of exotic trees for industrial and agricultural purposes are burgeoning in the tropics, andsome of them offer the opportunity to study community ecology of animals in a simplified forest set-ting. We examined bird community assembly in different aged groves of the industrial tree mangium(Acacia mangium) at two plantations in Malaysian Borneo: Sabah Softwoods near Tawau, Sabah, andthe Planted Forest Project, near Bintulu, Sarawak. Bird communities were compared among three age-groups of mangium (2-, 5-, and 7-years old) and logged native forest. Mangium rapidly developed intoa secondary forest consisting of a wide diversity of understory trees and shrubs. The bird communitycorrespondingly increased in species richness and diversity, and we were able to relate these increasesspecifically to canopy height, secondary canopy development, and shrub cover. Species of common, smallbodied frugivores, nectarivores, and insectivores were diverse in older plantation groves, as were com-mon mid-sized insectivores. However, large, specialized, and normally uncommon taxa (e.g., galliforms,pigeons, hornbills, barbets, midsized woodpeckers, muscicapine flycatchers, and wren babblers) wererare or nonexistent in the plantations. Because we lacked species-specific data on foraging, nesting, andother behaviors of most groups of birds, it was difficult to explain the precise causes of seral diversifica-tion in any group except woodpeckers, which have been well studied in Southeast Asia. Thus, in future,particular emphasis needs to be placed on obtaining such data. Industrial plantations, by virtue of theirsimple structure, variably aged groves, and bird community richness, are good places to gather such data.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

“Industrial” plantations that produce fast growing trees for pulp,composite board, and solid wood products are burgeoning in thetropics worldwide (Cossalter and Pye-Smith, 2003; Dvorak, 2004;Evans, 2009). Because of concern that monocultures of exotic treeswill have an adverse effect on biodiversity (Fitzherbert et al., 2008;Sodhi et al., 2008), research on native animals in tropical planta-

∗ Corresponding author at: Louisiana State University, Museum of Natural Science,119 Foster Hall, Baton Rouge, LA 70808, United States. Tel.: +1 225 578 2887;fax: +1 225 578 3075.

E-mail addresses: [email protected] (A.R. Styring), [email protected](R. Ragai), junis [email protected] (J. Unggang), [email protected] (R. Stuebing),[email protected] (P.A. Hosner), [email protected] (F.H. Sheldon).

1 Tel.: +1 360 867 6837; fax: +1 360 867 5430.2 Tel.: +62 086 335880; fax: +62 086 335890.3 Tel.: +62 541 732898; fax: +62 541 732537.4 Tel.: +1 785 864 3657; fax: +1 785 864 5335.

tions is also burgeoning (Barlow et al., 2007; Rotenberg, 2007; Koh,2008; Sheldon et al., 2010). However, most of these studies havefocused on determining which kinds of animals occur in planta-tions. Relatively few have taken advantage of plantation structureto study animal ecology, especially community succession. This issurprising because some types of plantations offer a natural exper-iment in community assembly. The occurrence of different agedgroves of trees at a single location allows the examination of avariety of seral stages at a single point in time and space (e.g.,Atkeson and Johnson, 1979; Mitra and Sheldon, 1993; Hanowskiet al., 1997; Koh, 2008). This “space-for-time” approach, and theresulting “chronosequence” of observations (Pickett, 1989), allowsbiologists to compare habitat and community characteristics of col-onizing species, as long as a plantation’s groves develop adequatebotanical complexity during their relatively short existence. Indus-trial tree plantations in the tropics are often well suited for suchstudies because they comprise extremely fast growing trees thatcan develop rich secondary understories (Mitra and Sheldon, 1993).Agricultural plantations, such as oil palm (Elaeis guineensis), how-

0378-1127/$ – see front matter © 2010 Elsevier B.V. All rights reserved.doi:10.1016/j.foreco.2010.11.003


532 A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544

Fig. 1. Sarawak Planted Forest Project and Sabah Softwoods plantations. Numbers refer to transect sites listed in Appendix A.

ever, tend not to be as useful because their undergrowth is moreintensively managed and, thus, unusually depauperate in botanicaland animal community structure (Koh, 2008; Sheldon et al., 2010).As long as investigators recognize that seral studies in plantationsoffer a simplified view of complicated processes, such studies havethe potential to provide insight into important ecological questions,especially how so many species are able to coexist in tropical rain-forest (Klopfer and MacArthur, 1961; Karr, 1971). Moreover, suchstudies should benefit conservation efforts by providing develop-ers with information on community ecology that can be translatedinto plantation design and management to encourage biodiversity(Hanowski et al., 1997; Stuebing, 2007; Nasi et al., 2008).

In ornithology, most efforts to understand rainforest bird com-munity succession have focused on chronosequences in naturalforest (Terborgh, 1985), logged or burned forests of different ages(e.g., Lambert, 1992; Johns, 1996; Barlow and Peres, 2004; Styringand Zakaria, 2004a), or forest recovering from slash-and-burn agri-culture (e.g., Bowman et al., 1990; Blankespoor, 1991; Ramanet al., 1998; Borges, 2007). The potential for insight from theseapproaches is substantial because each examines change or recov-ery of native forest, and native forest is richer than exotic forest incompositional and structural information. This is particularly trueof studies of natural forest and slash-and-burn succession becausechronosequences may span hundreds of years. However, workingwith native systems is difficult. There may be uncertainty aboutthe age and sequence of seral stages, or a lack of replicate plotsof the same age, or unclear borders between age groups. Researchin natural forest is particularly difficult because it requires a hugeinvestment of time to understand the terrain and birds (Terborgh,1985; Terborgh et al., 1990). Forest recovering from human pertur-bation has the additional problem that plots may have experienceddifferent forms and intensity of disturbance (Johns, 1997; Ramanet al., 1998). Although studies of bird community succession inplantations are limited in scope and reality relative to those innative forest, they still provide information on habitat differencesthat influence the occurrence and distribution of birds.

We studied bird community development at two industrial treeplantations in Malaysian Borneo. The first was Sabah SoftwoodsSdn. Bhd. (hereafter SS). This plantation is located ca. 50 km NNWof Tawau in the Tawau District of southeastern Sabah (Fig. 1) andis administered from Brumas Camp (4◦30′N, 117◦′E; ca. 300 m ele-vation). SS was established in 1974 and covers about 60,000 ha, ofwhich some 35,000–40,000 ha are planted with exotic trees includ-ing mangium (Acacia mangium), Albizia (Paraserianthes falcataria),white teak (Gmelina arborea), and oil palm (E. guineensis) (Pinsoand Vun, 2000). Several faunal studies have been conducted at SS(e.g., Duff et al., 1984; Stuebing and Gasis, 1989; Mitra and Sheldon,1993; Sheldon et al., 2010), and lists of birds found in native forest atthat site have been compiled periodically since 1977 (Sheldon et al.,2001). The second plantation is the Sarawak Planted Forest Project(hereafter PFP), located ca. 30 km S of Bintulu in the Tatau District ofcentral Sarawak (Fig. 1). Its administrative center is the SamarakanNursery (2◦56′N, 113◦07′E; ca. 50 m elevation). The PFP was estab-lished in the mid-1990s, when the Sarawak government set asidesome 500,000 ha for forest development projects. About 200,000 hahave been planted with mangium (Stuebing, 2005). Like SS, the PFPhas been the focus of several faunal studies (e.g., Stuebing et al.,2007; Shadbolt and Ragai, 2010), and lists of birds in the PFP havebeen compiled continuously since January 2005 (Stuebing, 2007).

The groves we examined for this study comprised loggednative forest and three age-groups of mangium. Our surveys weredesigned to estimate bird species richness (number of species),diversity (number of species adjusted for abundance of individualsin each), and density (individuals/hectare) occurring in each grovetype. Because we expected bird and plant community complex-ity to be correlated (MacArthur and MacArthur, 1961; Roth, 1976;Hanowski et al., 1997; Rotenberg, 2007), we related bird occur-rence in each grove to the physical structure of the grove, includingits canopy height and cover and the extent of its understory. Birdcommunities occurring in logged native forest patches within theplantations served as points of reference as we assessed severalmeasures of community structure across plantation age and looked


A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 533

for overarching patterns. Our fundamental goals were to determinewhich species are early colonizers and which are late, and to assessthe relationship between species composition and microhabitat.Eventually, with further study of foraging and food, the main goalwill be to evaluate how morphologically similar, sympatric con-geners coexist in Bornean rainforest.

2. Methods

Surveys at SS were conducted from 23 June to 12 July 2005 infour grove (or habitat) types: logged native forest, and 2-year-old,5-year-old, and 7-year-old mangium. Surveys in the PFP were con-ducted from 19 July to 9 August 2006 in the same four habitats. Thelogged native forest at SS was located on hills within the plantationthat were too steep for silviculture. This forest was logged lightly inthe 1980s and again in the 1990s, thus it exemplified upland sec-ondary forest. The logged native forest in the PFP was retained byplantation developers as a buffer for the benefit of wildlife. The sec-tion we surveyed is the “Bukit Mina Conservation Corridor” (Fig. 1).It had been logged selectively multiple times since the 1970s and,prior to that, was subject to shifting cultivation. It now consistsmainly of old, lowland secondary riverine forest, running in a ca.1 km wide strip across the center of part of the plantation.

Point counts were conducted in both plantations along tran-sects using distance sampling (Buckland et al., 2001). Transectswere randomly situated in each habitat type (Fig. 1). Each transectwas 1000 m long and consisted of 20 points, each 50 m apart. Pointswere spaced relatively closely together to provide a comprehensiveinventory. A three-minute bird survey was conducted and habitatdata were collected at each point. Characteristics of SS mangiumand logged forest are provided in Sheldon et al. (2010). The numberof transects varied among habitat types: 5–6 transects in differentages of mangium, 6 transects in logged forest at SS, and 12 tran-sects in logged forest at PFP (Appendix A). The close spacing ofpoints, while effective for estimating richness, increased the prob-ability of double counting individuals of common species. Beforeanalyzing the data, therefore, we ran summary statistics on detec-tion distances using R 2.7.2 (Murdoch, 2008). The optimal distancebetween points was determined by establishing the 95% detectionradius around each point. We then selected one of the 20 points ina transect using a random number table and spaced other pointsaccordingly. Observations were truncated at one half of the pointspacing interval. This subset of samples and observations formedthe dataset for all subsequent analyses.

Species accumulation curves, jackknifed estimates of diversity,mean point species richness, and Shannon’s Diversity indices (H′)were produced using PC-Ord 5 (McCune and Mefford, 2006). Toexamine the influence of feeding preference on habitat selection,we divided species into feeding guilds (Appendix B) using the classi-fication presented in Lambert (1992) and modified by Sheldon et al.(2010). To determine the influence of habitat preference on birddistribution, we also classified species by habitat using the groupsdefined by Rotenberg (2007) and information on habitat preferencefrom Lambert (1992) and Sheldon et al. (2001). The groups were:FS, forest specialists; ETF, edge tolerant forest specialists; ES, edgespecialists; OS, open country species; G, generalists; and O, other.Mosaic plots were then constructed with JMP 7.0.2 (SAS, 2008) tocompare distributions of feeding guilds and habitat types acrossdifferent groves types.

We estimated bird density within each habitat type at eachsite using Distance 6.0 (Thomas et al., 2006). Distance derives itsestimates from a detection function of measured distances (radialdistance in the case of point counts) of individual birds from theobserver. The estimates are accurate and robust if the follow-ing assumptions are met: (1) all individuals at distance zero are

observed, (2) movement of the target organism is not in responseto movement of the observer, and (3) distances are measuredaccurately (Thomas et al., 2002). Our surveys were designed tomeet these assumptions. We approached each point quietly andwaited several minutes before conducting counts. This allowedany birds that had stopped singing or had moved away to resettle.We measured distances with tilt-compensated laser rangefinders.Although it was sometimes difficult to determine exactly wherean individual was located, we made every effort to ensure preciseand accurate measurements by mapping and measuring significantlandscape and habitat features near the point prior to the survey,mapping bird locations in relation to those features during the sur-vey, and periodic ground-truthing to ensure measurements withour rangefinders were accurate. In dense vegetation, it was diffi-cult to say with 100% confidence that all individuals at distancezero were detected, but observers were trained to focus atten-tion on and near point zero during the survey. Encounter rateswere estimated from individual points and detection probabilitywas modeled and estimated by habitat type and site. Encounterrates, detection probability and density estimates were calculatedby habitat. We selected the half-normal key function with a cosineexpansion. Cosine adjustments were made sequentially and eval-uated using Aikake’s Information Criterion (AIC) (Thomas et al.,2010).

Because of the theoretical expectation that biomass shouldincrease with forest maturity (Odum, 1969), we examined therelationship between forest type and mass of its bird community.The average mass of most bird species was computed from Sabahspecimens at the Western Foundation of Vertebrate Zoology, LosAngeles, California (Sheldon et al., 2001). For a few species (<10),mass was estimated from information in the Handbook of Birds ofthe World or on-line sources. We compared masses between SS andPFP and among habitats within each plantation using T-tests andone-way ANOVA (using JMP), with post hoc comparisons usingTukey–Kramer’s HSD. Because the data were strongly skewed,such that large species were orders of magnitude heavier than themedian-sized species, the data were log transformed. This reducedskewness significantly, but some very large species still influencedthe data. Therefore, in addition to running ANOVA on the log-transformed data, we computed an equivalent non-parametric test(Kruskall–Wallis) for comparison.

Nonmetric multidimensional scaling was performed in PC-ordto detect patterns in bird community structure related to habitattype. We also conducted a randomization procedure (100 runs)to determine the optimal number of dimensions to be used inthe ordination. Data were relativized by maximum to reduce theinfluence of rare species, which can skew ordination results dis-proportionately (McCune and Mefford, 1999). NMS was performedusing Bray–Curtis as the distance metric, 1000 runs with real data, astability criterion of 0.0005, and 500 maximum iterations (509 wasthe randomly selected start point generated by the analysis). Corre-lation between individual species and overall community structurewas determined using Pearson’s correlation coefficients. Correla-tions with an r-squared value greater than 0.20 on any one of thefirst two axes were considered significant and were plotted onto theordination as an overlay. A multiple response permutation proce-dure (MRPP) was also performed in PC-ord to determine variationin bird community composition among habitat types.

3. Results

We conducted 985 point counts of birds and surveys of habitatat SS and PFP (455 and 530, respectively) and recorded a total of 111bird species (Appendix B). Because our ability to detect individualbirds differed among habitats, we established point-spacing based



Table 1Sampling and detection statistics.

Plantation Habitat Initial samplingeffort (no. points)

95% detectionradius (m)

Subsequentspacing of points

Resulting samplingeffort (no. points)

Sabah Softwoods 2-y mangium 99 70 150 355-y mangium 119 75 150 367-y mangium 120 81.2 200 30Logged forest 117 88.8 200 29

Sarawak PFP 2-y mangium 88 106.6 250 185-y mangium 100 106.6 250 207-y mangium 120 91 200 30Logged forest 222 127 300 32

on bird detectability (Table 1). This resulted in the use of pointsbetween 150 and 300 m apart and a substantial reduction in pointsanalyzed compared to points sampled (130 for SS; 100 for PFP).By reducing the sample, we minimized the possibility of double-counting individual birds.

Species richness, abundance, diversity, mass, and density aresummarized in Tables 2 and 3 and Figs. 2 and 3. Bird speciesin mangium increased in richness, abundance, and diversity withincreasing age. Per point species richness and diversity was sim-ilar and even slightly higher in older mangium compared tologged forest. However, overall estimates of species richness andspecies accumulation rates were much higher in the logged for-est, indicating a higher species turnover rate between points inlogged forest. Bird density and mass did not increase with plan-tation age, but were significantly higher in logged forest comparedto plantation. For bird mass, ANOVA and Kruskal–Wallis testsyielded congruent results. Variation in bird mass among habitatswas significant: ANOVA, F = 21.2, p < 0.0001; Kruskal–Wallis, Chi-square = 53.0, p < 0.0001. Tukey–Kramer’s pairwise comparisons

Table 3Bird density estimates (individuals/hectare) for mangium (Acacia mangium) andlogged forest at Sabah Softwoods (SS) and the Sarawak Planted Forest Project (PFP).%CV is the coefficient of variation expressed as a percentage, and L 95 and U 95 arethe lower and upper 95% confidence estimates.

Mean %CV L 95 U 95

2-y mangium 13.2 12.8 10.3 17.05-y mangium 11.9 16.7 8.6 16.57-y mangium 13.7 11.2 11.0 17.0Logged forest 19.9 8.6 16.9 23.6

indicated that birds in different plantation age-groups did not differsignificantly in size, but those in logged native forest were larger onaverage than those in mangium (p < 0.05). This was largely due togreater abundance of some very large-bodied birds in logged forest(e.g., pheasants, raptors, hornbills, and large woodpeckers).

The distribution of foraging guilds differed significantly acrosshabitats: SS Likelihood Ratio Chi-square = 275.1 p < 0.0001 (Fig. 4).In general, the number of guilds increased with plantation age,

Table 2Summary statistics for bird communities in mangium (Acacia mangium) and logged forest.

Habitat Observed species richness (andJackknifed estimates of richness)

Per-point speciesrichness

Per-pointabundance

Per-point diversity(H′)

Mass mean (SD), median

2-y mangium 36 (51–63) 4.9 8.0 1.41 21.9 (43.7), 15.45-y mangium 53 (72–84) 5.7 8.3 1.59 24.8 (59.1), 15.47-y mangium 62 (85–95) 6.6 9.0 1.76 22.8 (48.8), 15.4Logged forest 92 (120–131) 5.9 9.4 1.54 61.7 (229.1), 19.26

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Fig. 2. Species accumulation curves by habitat type.



12-year Acacia 5-year Acacia Logged Forest7-year Acacia

Age (grouped)

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s (l

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)

Fig. 3. One-way comparison of log bird mass by habitat. The center of each diamondrepresents the mean and lines at the tips the 95% confidence interval. The barswithin and near the tip of each diamond indicate the overlap in means (calculated

as mean ± ((√

2)/2 × CI/2).

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Fig. 4. Mosaic plot of bird feeding guilds by habitat. The height of each coloredsection reflects the proportion of individuals in a particular guild in that habi-tat. The width of each column reflects sample size. The main guilds shown hereare: black (AF) arboreal frugivore, gray (AFGI) arboreal foliage gleaning insecti-vore, blue (AFGIF) arboreal foliage gleaning insectivore–frugivore, light blue (NI)nectarivore–insectivore, red (NIF) nectarivore–insectivore–frugivore, white (SI) sal-lying insectivore, yellow (SSGI) sallying substrate-gleaning insectivore, and green(TI) terrestrial insectivore. See Appendix B for the complete classification of species’guilds. (For interpretation of the references to color in this figure legend, the readeris referred to the web version of the article.)

and logged forest had the greatest guild complexity. Two-yearmangium contained eight foraging guilds, but was overwhelminglydominated by two: arboreal foliage gleaning insectivores (Prinia fla-viventris, tailorbirds, and Macronous bornensis) and arboreal foliagegleaning insectivore/frugivores (mainly bulbuls). The bird commu-nities of 5-y and 7-y mangium included 9–10 guilds, 6 of whichwere well represented. Four of these guilds were still dominatedby just a few species: terrestrial insectivores (mainly Pellorneumcapistratum and Malacocincla malaccensis); sallying insectivores(mainly Rhipidura javanica); nectarivore-insectivore–frugivores(mainly Prionochilus xanothopygius and Dicaeum trigonostigma);

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Fig. 5. Mosaic plot of avian microhabitat preferences by habitat. The height of eachcolored section reflects the proportion of individuals in a particular guild in thathabitat. The width of each column reflects sample size. The microhabitat classes(from Rotenberg, 2007) are: gray (ES) edge specialist, black (ETF) edge tolerant for-est specialist, yellow (FS) forest specialist, blue (G) generalist, and white (OS) opencountry species. (For interpretation of the references to color in this figure legend,the reader is referred to the web version of the article.)

nectarivore–insectivores (mainly Arachnothera longirostra). Thetwo other guilds were relatively large and diverse: arboreal foliagegleaning insectivores (mainly tailorbirds and a few species of bab-blers) and arboreal foliage gleaning insectivore-frugivores (mainlybulbuls). Logged forest communities comprised 12–14 guilds.These were more evenly distributed than guilds in the planta-tion; they were no longer dominated by a few species of bulbuls,tailorbirds, and babblers. Logged forest also featured a substan-tial increase in sallying substrate-gleaning insectivores, whichare large midstory species such as trogons, broadbills, and dron-gos. For microhabitat classes, a similar pattern of increasing birdcommunity complexity was evident: SS Likelihood Ratio Chi-square = 365.7, p < 0.0001 (Fig. 5). Although all habitat types weredominated by birds favoring forest edge, 7-y mangium and espe-cially logged forest included a more substantial proportion of forestspecialists (e.g., Erpornis zantholeuca, Stachyris poliocephala, Mala-copteron cinereum, and Trichastoma bicolor).

NMS randomization (Fig. 6) indicated that two dimensions gen-erated the least stress in the ordination, and the final ordinationand MRPP reflected a clear differentiation between native forestand plantation (T = −16.0, A = 0.14, p < 0.0001), with native forestdiffering significantly from all plantation types (p ≤ 0.00000005).Although some overlap occurred among plantation samples, 2-year-old mangium differed significantly from older plantationsamples (p < 0.005). The most similar habitats were 5- and 7-year mangium (p = 0.25). Bird community structure was highlycorrelated with canopy height, secondary canopy height, percentsecondary canopy cover, and shrub height. These were key vari-ables in distinguishing logged forest communities from youngerplantation. Species that correlated strongly with the ordination(Fig. 7) included those found almost exclusively in native forest(Eurylaimus ochromalus, Harpactes kasumba, Megalaima australis,and Irena puella), species found primarily in native forest, butalso occurring in lower numbers in older plantation (Orthotomusatrogularis and Pycnonotus erythropthalmos), species found primar-ily in plantation (Macronous bornensis and Orthotomus sericeus),and species found primarily in young plantation and less fre-quently in older plantation (Pycnonotus goiavier and Rhipidurajavanica).



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s 2

2-year Acacia5-year Acacia7-year AcaciaLogged Forest

% Shrub cover

% Secondary canopy cover

Canopy height

Secondary canopy height

Fig. 6. NMS of survey data. Each dot corresponds to an individual survey transect used in the final analysis. The vectors indicate correlations between community structureand habitat variables with r-squared values greater than 0.5.

4. Discussion

4.1. Species assembly

In his classic paper on forest succession and Amazonian birddiversity, Terborgh (1985) listed key factors that influence habi-tat choice. These included: microclimate, foraging substrates, foodresources, nesting sites, cover, competition, predators, and para-sites. He noted that three of these factors—foraging substrates, foodresources, and competition—play especially important roles andcan be evaluated more readily than the others. Indeed, foragingsubstrates and food resources are assessed in most comparisonsof bird communities because they are easy to visualize and quan-tify; foraging substrates are defined by habitat structure, and foodresources can be observed indirectly by examining feeding guilds

(e.g., Lambert, 1992; Johns, 1996; Styring and Zakaria, 2004a; Pehet al., 2005; Edwards et al., 2009). Competition is more difficultto measure, but is suggested by seral changes in kinds and pro-portions of congeners or morphologically similar species. Terborgh(1985) also emphasized the interdependence of habitat-choicefactors. Food resources, foraging substrates, competition, microcli-mate, cover, nesting, etc., are all related to habitat complexity (e.g.,MacArthur and MacArthur, 1961; Bowman et al., 1990).

4.1.1. Foraging substratesWe examined some of these habitat-choice factors and detected

the expected trends: bird diversity was strongly associated withthe structural complexity of plantation groves. Structural complex-ity in mangium developed relatively quickly. The fast growing croptrees established a high canopy that provided space for a substantial

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2-year Acacia5-year Acacia7-year AcaciaLogged ForestCorrelated species

Rhipidura javanica (0.322,0.093)

Eurylaimus ochromalus(0.235,0.213)

Megalaima australis(0.126, 0.232)

Harpactes kasumba (0.207, 0.110)

Pycnonotus erythropthalmos(0.329,0.055)

Pycnonotus goiavier

(0.254,0.306 )

Macronous bornensis (0.587,0.091)

Orthotomus atrogularis(0.096, 0.227)

Orthotomus sericeus (0.462,0.026)

Irena puella(0.27, 0.00)

Fig. 7. NMS of survey data. Each dot corresponds to an individual survey transect used in the final analysis. Species that are correlated with the ordination (r-squared valuesgreater than 0.20) are plotted. Numbers in parentheses are r-squared values for axis 1 and axis 2, respectively.



understory in five years and sometimes even a distinct midstory inseven years (Sheldon et al., 2010). On the other hand, 2-y mangiumlacked a canopy and featured largely an open, grass and fern under-story. NMS randomization showed that canopy height, secondarycanopy height, percent secondary canopy cover, and shrub heightwere the key variables distinguishing bird communities amonghabitats (Fig. 6). Number of feeding guilds (Fig. 4) and forest spe-cialist species (Fig. 5) increased with time, and guilds became moreevenly distributed, presumably because the variety and spatial dis-tribution of food resources increased as the plantation becamemore forest-like.

Such results are largely intuitive and do not explain in anydetail what happens in the bird community as the forest matures.It would be much more satisfying to know what each individ-ual bird species is doing relative to others. However, this is notan easy task because so little information exists about the micro-habitat requirements and interactions of Bornean forest species.No quantitative, comparative foraging or nesting studies exist forthe plantation’s most common species: bulbuls, tailorbirds, andbabblers. In fact, the only forest group in insular Southeast Asiafor which we have quantitative comparative foraging information,other than hornbills (Leighton, 1982), is woodpeckers (Styring andIckes, 2001a; Styring, 2003; Lammertink, 2004; Styring and Zakaria,2004b,a). Nevertheless, NMS provided a quantitative assessment ofseral changes in a few groups of birds as the plantation aged or wasreplaced by native forest (Fig. 7).

Of the ten species that exhibited abundance patterns that werecorrelated strongly with NMS ordination (Fig. 7), two pairs (O.sericeus and O. atrogularis, and P. goiavier and P. erythropthalmos)consisted of congeners that replace one another through time.O. sericeus occurred in low numbers in young groves, unusuallylarge numbers in older groves, and low numbers in logged forest(Appendix B). O. atrogularis was rare in young plantation, morecommon in the older groves, and very common in logged forest.A third species, O. ruficeps, is common in all ages of plantation, butoccurs in lower numbers in logged forest. A total of seven bulbulsin the genus Pycnonotus were found in both sites. P. goiavier wasmost abundant in young plantation. It was increasingly replaced inolder plantation groves by P. simplex and P. erythropthalmos, bothof which were common in logged forest (Appendix B). P. brun-neus and P. atriceps exhibited conflicting patterns between the twoplantations, and P. cyaniventris only occurred in logged forest. Twoadditional pairs of congeners—M. bornensis and M. ptilosus, and R.javanica and R. perlata–appeared to replace one another throughtime (Appendix B), but only the occurrence of the early colonist (M.bornensis and R. javanica) was significantly correlated with foresttype (Fig. 7).

Woodpecker occurrence in mangium provided qualitativeinsight into the interplay between habitat structure and bird com-munity assembly. In young plantation, the only woodpeckers thatoccurred in any numbers were small bodied branch-gleaners,Sasia abnormis and Meiglyptes tristis, and the ant-termite special-ist, Micropternus brachyurus (Appendix B). As the plantation aged,trunk specialists (e.g., Blythipicus rubiginosus, Picus puniceus, andDryocopus javensis) started to appear, attracted by an increasingnumber of dead and insect-infested trees for foraging and by larger,soft-wood boles for nest excavation (Wells, 1999; Styring andZakaria, 2004b; Sheldon et al., 2010). Some species that were notrecorded in the plantation (e.g., Reinwardtipicus validus and Picusmentalis) require a combination of foraging and nesting habitatand canopy cover not met in mangium (Styring and Ickes, 2001b;Styring and Zakaria, 2004b).

A variety of other foraging substrates appeared in older planta-tion groves. A distinct, flat canopy developed in 5-y and especially7-y mangium, and this was frequented by gleaning insectivores inrelatively large numbers, e.g., the iora Aegithina viridissima and the

white-eye Zosterops everetti. Also, mangium produces seed podsonce a year that contain small black seeds with oily orange funi-cles that attract some small frugivores. The flat canopy of mangiumdiffers from that of native forest in lacking emergents and largefigs. Thus, some canopy specialists, especially large frugivores (e.g.,pigeons, hornbills, and barbets) were rare in the mangium. Sub-canopy development (Fig. 6) in 5-y and 7-y mangium attractednumerous large bodied foragers: e.g., malkohas (Phaenicophaeuschlorophaeus and P. curvirostris), trogons (Harpactes diardii), a king-fisher (Ceyx rufidorsum), and some broadbills (Calyptomena viridisand Eurylaimus ochromalus). Most of these feed on large arthropods,although C. viridis is a frugivore. Like woodpeckers, these specieswere also attracted to nesting opportunities on older groves (e.g.,H. diardii was observed nesting in a hole in a 7-year mangium snag).The more open understory of older groves also permitted occupa-tion by a few flycatchers, e.g., Hypothymis azurea and Terpsiphoneparadise, but most flycatchers eschewed the plantation (Mitra andSheldon, 1993; Sheldon et al., 2010). The most dramatic increase inspecies in mangium occurred in response to the development of lowshrubs and ground cover. Species associated with these substratesforage by gleaning or thrashing and included the thrush Copsychusmalabaricus and several forest babblers (Stachyris erythoptera, S.maculata, Macronous ptilosus, Pellorneum capistratum, Malacocinclamalaccensis, Trichastoma bicolor, and T. rostratum). Most of thesespecies also nest in the plantation (Sheldon et al., 2001; personalobservation).

4.1.2. Food resourcesWithout specific knowledge of arthropod communities, we

have relied on changes in forest structure and feeding guilds(Figs. 4 and 6) to suggest increasing food resources for insec-tivores and omnivores as the plantation ages. For frugivoresand nectarivores, we have more information on potential foodsources (e.g., Kuusipalo et al., 1995; Otsamo, 2000; B. Tan, pers.comm.).

Groves of 2-y mangium were essentially fields of grass, ferns,and some shrubs (mostly Chromolaena odorata) filled with saplingmangiums. Bird food was presumably limited largely to insects andseeds, and the bird community was dominated by a few abundantspecies (Appendix B): especially, the omnivorous bulbul P. goiavierand some foliage gleaning insectivores—the babbler M. bornensisand three warblers, Orthotomus ruficeps, O. sericeus, and P. flaviven-tris. Granivores (e.g., Lonchura spp.) that would feed on grass seedswere rare; instead these were mainly exploited by P. goiavier. Afew more bird species would be expected in 2-y mangium duringDecember to March, as seasonal rains increase flowering and fruit-ing and migrants visit from mainland Asia. In general, the opencountry avifauna of Borneo is depauperate, as it is in New Guinea(Bowman et al., 1990), contrasting with relative species richnessin cleared areas of tropical Africa and the Neotropics, which havemore diverse savanna avifaunas.

In mature mangium, secondary flora that attracted frugivoresand nectarivores became diverse. The midstory of older groves caninclude more than 60 tree species in some 24 families, includingmany varieties of fruiting trees, such as Vitex pubscens (Verbe-naceae), Alstonia angustiloba (Apocynaceae), Ficus grossularioides(Moraceae), Anthocephalus chinensis (Rubiaceae), Trema tormentosa(Cannabaceae), Dillenia suffruticosa (Dilleniaceae), and Macarangaand Mallotus (Euphorbiaceae) (Mitra and Sheldon, 1993; Kuusipaloet al., 1995; Otsamo, 2000). Most of these are secondary forestspecies imported by birds and bats that presumably rest in theplantation canopy (Kuusipalo et al., 1995). Some of these trees,e.g., Trema, Mallotus and Macaranga, provide fruit throughout theyear, thus supporting small-bodied birds fairly continuously. Figs,on the other hand, which are the main food of large frugivoresin primary forest, have short fruit-production periods, and many



individual fig trees are required to support species that dependon them (Zakaria and Nordin, 1998). Thus, pigeons, hornbills, andbarbets cannot feed solely within mangium and, with the excep-tion of the terrestrial dove Chalcophaps indica, were rare in theplantation. There were also numerous fruiting and nectar-bearingshrubs in the plantation, including: Plagiostachys, Hornstedtiascyphifera, and Etlingera (Zingiberaceae); Knema (Myristicaceae);Schumannianthus monophyllus and Stachyphrynium (Marantaceae);Gardenia sp. (Rubiaceae); Tacca integrifolia (Dioscoreaceae),Helminthostachys zeylanica (Ophioglossaceae); and Litsea sp. (Lau-raceae). The gingers and Tacca are well documented as feedingplants for nectarivores, and Knema and Litsea produce fruits eatenby hornbills and presumably many other frugivores (Sakai et al.,1999; besgroup.talfrynature.com).

Although the connection between the proliferation of fruit-bearing trees and frugivores is clear (Fig. 4), the complexitiesof interaction are not. Particular bird species cannot be linkedto specific fruit because most fruiting trees attract multiple birdspecies and the interaction of birds and trees is largely proba-bilistic. However, we detected species changes in the frugivorecommunity (Fig. 7, Appendix B). For example, the generalist P.goiavier was continuously replaced through time by an increas-ing number of bulbul species and other medium-sized frugivores,e.g., C. viridis, Gracula religiosa, Pycnonotus atriceps, P. brun-neus, P. simplex, and P. erythropthalmos. A similar increase innectarivore diversity occurred. In the young plantation the dom-inant species were the sunbirds Anthreptes malaccensis, Aethopygasiparaja and Arachnothera longirostra and the flowerpeckers Pri-onochilus xanthopygius and Dicaeum trigonostigma. These speciesincreased in abundance as the plantation aged and were joinedby other nectarivores: e.g., Anthreptes rhodolaema, A. singalensis,Leptocoma brasiliana, Hypogramma hypogrammicum, and Dicaeumconcolor.

4.2. Biomass

In theory, biomass of individual species should increase withforest age, as selective advantage shifts to larger organisms thathave more complex life histories and which live longer in therelatively stable environment of mature forest (Odum, 1969). How-ever, this expected pattern is not always found empirically (Bockand Lynch, 1970; Helle, 1985). We did not detect a size changeas the plantation age, probably because the amount of time (7years) was inadequate for a substantial change to develop. Wedid find, however, that biomass of individual bird species andvariation in size among species were on average much higher inlogged native forest than in exotic tree groves (Fig. 3); the loggedforest housed not only many small and medium-sized birds, butalso unusually large ones, e.g., pheasants, trogons and hornbills.These differences make sense in light of the greater variation infood and nesting resources in native forest versus the plantation(Fig. 6).

5. Future work

Future work on birds in Southeast Asian industrial tree plan-tations needs to emphasize two kinds of studies: (1) comparativeecology of species in potentially competing groups (especially bul-buls, babblers, and tailorbirds), and (2) landscape comparisons thatexamine the mutual influence of adjacent plantation and nativeforest communities. Community studies need to collect compara-tive data on foraging, food, nesting, and interspecific interaction.The simple structure of plantation forests and limited numbers ofbird species should make it relatively easy to detect more preciselythe needs of potentially competing taxa. Landscape effects areespecially important to understanding community assembly andimproving conservation planning (Renjifo, 2001; Pearman, 2002;Luck and Daily, 2003; Barlow and Peres, 2004; Edwards et al.,2010). Communities in adjacent habitats influence one anotherin both directions, either from the native forest into plantation(Raman, 2006; Koh, 2008; Sheldon et al., 2010) or vice versa (Ickeset al., 2005). In this study, we attempted to minimize landscapeeffects by positioning transects as far as possible from adjacenthabitats, and by comparing two plantations that occupied differ-ent locations (550 km apart) and landscapes (PFP in flat lowlandsat ca. 50 m in elevation versus SS in rolling uplands at ca. 300 m).Nevertheless, landscape influence is pervasive and important toplantation-development planning.

Acknowledgments

We thank the Planted Forest Project, Grand Perfect Sdn. Bhd.,and Sabah Softwoods Sdn. Bhd. for their kind hospitality and exten-sive logistical support of our research. We particularly thank: atSabah Softwoods Mohd. Hatta Jaafar, Elizabeth Bacamenta, Man-suit Gamallang, Allison Kabi, Mustapha Pai, and George Tham;and at the Sarawak Planted Forest Project Tony Chaong, RobertDerong, Belden Giman, Last Gundie, Diana James, Azizan Juhin,Joseph Li, Nyegang Megom, Henry Nyegang, Steven Stone, JimmyTeo, and Latiffah Waini. For technical advice on plants, we thankDr. Benito Tan, Paul Leong, and Serena Lee of the Herbarium ofthe Singapore Botanical Gardens. Permission to undertake researchin Sabah was provided by the Malaysian Economic Planning Unitof the Prime Minister’s Department, and help with research inthe State has been continuously aided by Sabah Wildlife Depart-ment (Datuk Mahedi Andau, Laurentius Ambu, Augustine Tuuga,and Peter Malim), Sabah Parks (Datuk Lamri Ali, Dr. Jamili Nais,and Maklarin Lakim), and Sabah Museum (Datuk Joseph Guntavid,Jaffit Majuakim, and Albert Lo). Permission to undertake researchin Sarawak was provided by the Sarawak Forestry Department,Sarawak Forestry Corporation, and Sarawak Biodiversity Centre.The research was funded by the Coypu Foundation of Louisiana,Disney Worldwide Conservation Fund, Grand Perfect Sdn. Bhd.,Louisiana State University, Sabah Softwoods Sdn. Bhd, and TheEvergreen State College.



Appendix A.

Transects conducted at Sabah Softwoods and the Sarawak Planted Forest Project.Transect Habitat Plot age (in years) or characteristics Survey date Surveyor

Sabah Softwoods1. AM2Y1 Acacia mangium 2 23-June-05 FHS/PAH2. AM2Y2 Acacia mangium 2 27-June-05 FHS3. AM2Y3 Acacia mangium 2 28-June-05 FHS4. AM2Y4 Acacia mangium 2 5-July-05 FHS5. AM3Y1 Acacia mangium 2 12-July-05 FHS6. AM5Y1 Acacia mangium 5 25-June-05 PAH7. AM5Y2 Acacia mangium 5 29-June-05 PAH8. AM5Y3 Acacia mangium 5 30-June-05 FHS9. AM5Y4 Acacia mangium 5 6-July-05 FHS10. AM5Y5 Acacia mangium 5 10-July-05 FHS11. AM5Y6 Acacia mangium 5 11-July-05 FHS12. AM7Y1 Acacia mangium 7 24-June-05 FHS/PAH13, AM7Y2 Acacia mangium 7 30-June-05 PAH14. AM7Y3 Acacia mangium 7 7-July-05 PAH15. AM7Y4 Acacia mangium 7 8-July-05 PAH16. AM7Y5 Acacia mangium 7 10-July-05 PAH17. AM7Y6 Acacia mangium 7 12-July-05 PAH18. LF1 Logged native forest Secondary hill forest 28-June-05 PAH19. LF2 Logged native forest Secondary hill forest 4-July-05 PAH20. LF3 Logged native forest Secondary hill forest 5-July-05 PAH21. LF4 Logged native forest Secondary hill forest 6-July-05 PAH22. LF5 Logged native forest Secondary hill forest 9-July-05 PAH23. LF6 Logged native forest Secondary hill forest 9-July-05 FHS

Sarawak Planted Forest Project1. AM2Y1 Acacia mangium 2 19-July-06 ARS2. AM2Y2 Acacia mangium 2 28-July-06 FHS3. AM2Y3 Acacia mangium 2 28-July-06 ARS4. AM2Y4 Acacia mangium 2 29-July-06 FHS5. AM2Y5 Acacia mangium 2 29-July-06 ARS6. AM5Y1 Acacia mangium 5 20-July-06 ARS7. AM5Y2 Acacia mangium 5 30-July-06 FHS8. AM5Y3 Acacia mangium 5 30-July-06 ARS9. AM5Y4 Acacia mangium 5 1-August-06 FHS10. AM5Y5 Acacia mangium 5 1-August-06 ARS11. AM7Y1 Acacia mangium 7 26-July-06 FHS12. AM7Y2 Acacia mangium 7 26-July-06 ARS13. AM7Y3 Acacia mangium 7 27-July-06 FHS14. AM7Y4 Acacia mangium 7 27-July-06 ARS15. AM7Y5 Acacia mangium 7 31-July-06 FHS16. AM7Y6 Acacia mangium 7 31-July-06 ARS17. LF A1 Logged native forest Secondary riverine forest 21-July-06 ARS18. LF A2 Logged native forest Secondary riverine forest 22-July-06 ARS19. LF A3 Logged native forest Secondary riverine forest 23-July-06 ARS/FHS20. LF A4 Logged native forest Secondary riverine forest 24-July-06 ARS21. LF A5 Logged native forest Secondary riverine forest 25-July-06 ARS22. LF A6 Logged native forest Secondary riverine forest 24-July-06 FHS23. LF B1 Logged native forest Secondary riverine forest 3-August-06 FHS24. LF B2 Logged native forest Secondary riverine forest 3-August-06 ARS25. LF B3 Logged native forest Secondary riverine forest 4-August-06 FHS26. LF B4 Logged native forest Secondary riverine forest 4-August-06 ARS27. LF B5 Logged native forest Secondary riverine forest 5-August-06 FHS28. LF B6 Logged native forest Secondary riverine forest 5-August-06 ARS



Appendix B.

Non-migratory forest birds recorded in Sabah Softwoods (SS) and the Sarawak Planted Forest Project (PFP) in Acacia mangium (Acacia)and logged native forest (LNF).

Namesa Guildc Habitatd 2005 Survey SSe 2006 Survey PFPe

English Scientificb Acacia LNF Acacia LNF

2y 5y 7y 2y 5y 7y

Phasianidae: partridge, quail, and pheasantsScaly-breasted Partridge Arborophila charltoniiNT TIF FS 2 6Crested Fireback Lophura ignitaNT TIF FS 4 PGreat Argus Argusianus argusNT TIF FS 1 10 3

Accipitridae: hawks, eagles, and alliesJerdon’s Baza Aviceda jerdoni R ES P 2 POriental Honey-buzzard Pernis ptilorhynchus R ES P 1 2 PBat Hawk Macheiramphus alcinus R OS 2Brahminy Kite Haliastur indus R OS PLesser Fish-Eagle Ichthyophaga humilisNT R OS PCrested Serpent-Eagle Spilornis cheela R G 1 3 1 4 3 8Black Eagle Ictinaetus malayensis R OS 1Changeable Hawk-Eagle Spizaetus cirrhatus R G 1

Columbidae: pigeons and dovesEmerald Dove Chalcophaps indica TF ETF 9 13 11 15 1 8 1 4Jambu Fruit-Dove Ptilinopus jambuNT AF ETF 3Pink-necked Green Pigeon Treron vernans AF ETF PThick-billed Green Pigeon Treron curvirostra AF ETF 13 1 PGreen Imperial-Pigeon Ducula aenea AF FS 2 P

Psittacidae: parrots and parakeetsBlue-crowned Hanging-Parrot Loriculus galgulus NF ETF 2 1 12 16 1 5 1 16Blue-rumped Parrot Psittinus cyanurusNT AF FS 2 PLong-tailed Parakeet Psittacula longicaudaNT AF ETF 2 P

Cuculidae: old World cuckoosMoustached Hawk-Cuckoo Hierococcyx vagansNT AFGI FS PMalaysian Hawk-Cuckoo Hierococcyx fugax AFGI ETF 2 PIndian Cuckoo Cuculus micropterus AFGI OS PBanded Bay Cuckoo Cacomantis sonneratii AFGI ETF 9Plaintive Cuckoo Cacomantis merulinus AFGI G 21 4 4 1 24 2 8 PRusty-breasted Cuckoo Cacomantis sepulcralis AFGI ETF 1Violet Cuckoo Chrysococcyx xanthorhynchus AFGI ETF 1 6 1 3Little Bronze-Cuckoo Chrysococcyx minutillus AFGI ETF 1 1Drongo-Cuckoo Surniculus lugubris SI ETF 1 1 2Black-bellied Malkoha Phaenicophaeus diardiNT AFGI ETF PChestnut-bellied Malkoha Phaenicophaeus sumatranusNT AFGI ETF 1Raffles’s Malkoha Phaenicophaeus chlorophaeus AFGI ETF 3 1 7 9Chestnut-breasted Malkoha Phaenicophaeus curvirostris AFGI ETF 3 1 P 1 2Short-toed Coucal Centropus rectunguisVU AFGI FS PGreater Coucal Centropus sinensis TI OS 7 18 9 1 28 7 7 12Lesser Coucal Centropus bengalensis TI OS 22 3 P

Strigidae: typical owlsReddish Scops Owl Otus rufescensNT NP FS PSunda Scops Owl Otus lempiji NP FS PBarred Eagle Owl Bubo sumatranus NP ETF PBuffy Fish Owl Ketupa ketupu NP ES PBrown Wood Owl Strix leptogrammica NP FS PBrown Boobook Ninox scutulata NP FS P

Podargidae: frogmouthsGould’s Frogmouth Batrachostomus stellatusNT SSGI FS P

Caprimulgidae: nightjarsMalaysian Eared Nightjar Eurostopodus temminckii AI OS 3

Apodidae: swiftsGlossy Swiftlet Collocalia esculenta AI OS 2 P 1 P PSwiftlet Aerodramus sp? AI OS 2 P P P PSilver-rumped Needletail Rhaphidura leucopygialis AI OS 30 59Brown-backed Needletail Hirundapus giganteus AI OS PHouse Swift Apus affinis AI OS 1Grey-rumped Treeswift Hemiprocne longipennis AI OS 2 5Whiskered Treeswift Hemiprocne comata SI OS 14

Trogoniformes: TrogonidaeRed-naped Trogon Harpactes kasumbaNT SSGI FS 1 8 2 42Diard’s Trogon Harpactes diardiiNT SSGI FS 1 1 2 5 8 10



Appendix B. (Continued)



2y 5y 7y 2y 5y 7y

Cinnamon-rumped Trogon Harpactes orrhophaeusNT SSGI FS PScarlet-rumped Trogon Harpactes duvauceliiNT SSGI FS 1 12 1 2 2Coraciidae: RollersDollarbird Eurystomus orientalis SI OS P P

Alcedinidae: kingfishersBanded Kingfisher Lacedo pulchella MIP FS 1 5Stork-billed Kingfisher Halcyon capensis MIP OS PCollared Kingfisher Todiramphus chloris MIP OS 1 1Rufous-backed Kingfisher Ceyx rufidorsum SSGI FS 1 1 1 1 PBlue-eared Kingfisher Alcedo meninting MIP ETF 11Meropidae: Bee-eatersRed-bearded Bee-eater Nyctyornis amictus SI FS 2 1 4Blue-throated Bee-eater Merops viridis SI OS 2 11 P

Bucerotidae: hornbillsBushy-crested Hornbill Anorrhinus galeritus AFP FS 26 2Black Hornbill Anthracoceros malayanusNT AFP ETF 6 3 1 40Rhinoceros Hornbill Buceros rhinocerosNT AFP ETF 1 7 9Helmeted Hornbill Rhinoplax vigilNT AFP ETF 1 1 PWhite-crowned Hornbill Aceros comatusNT AFP FS PWreathed Hornbill Aceros undulatus AFP ETF 4 1

Capitonidae: barbetsGold-whiskered Barbet Megalaima chrysopogon AFP ETF 6 2 1 7Red-crowned Barbet Megalaima rafflesiiNT AF ETF 7 2Red-throated Barbet Megalaima mystacophanosNT AFGIF ETF 7 4 PYellow-crowned Barbet Megalaima henriciiNT AF ETF 1 6Blue-eared Barbet Megalaima australis AF G 9 2 1 37Brown Barbet Calorhamphus fuliginosus AFGIF ETF 4 22

Indicatoridae: honeyguidesMalaysian Honeyguide Indicator archipelagicusNT MI/P FS P

Picidae: woodpeckersRufous Piculet Sasia abnormis AFGI ETF 1 13 13 6 3 5 4 7Grey-capped Woodpecker Dendrocopos canicapillus AFGI ETF 3White-bellied Woodpecker Dryocopus javensis BGI ETF 2 10Rufous Woodpecker Micropternus brachyurus AFGI ETF 1 3 1 1 10Crimson-winged Woodpecker Picus puniceus BGI ETF 1 1 POlive-backed Woodpecker Dinopium rafflesiiNT BGI FS 1 1Maroon Woodpecker Blythipicus rubiginosus BGI ETF 3 1 1 3Orange-backed Woodpecker Reinwardtipicus validus BGI FS 4Buff-rumped Woodpecker Meiglyptes tristis AFGI ETF P 4 1 3 4 PBuff-necked Woodpecker Meiglyptes tukkiNT AFGI ETF 1 3 PGrey-and-buff Woodpecker Hemicircus concretus AFGI ETF 2 1

Eurylaimidae: broadbillsGreen Broadbill Calyptomena viridisNT AF FS 5 1 2 7Dusky Broadbills Corydon sumatranus SSGI ETF 2 3Black-and-red Broadbill Cymbirhynchus macrorhynchos SSGI OS PBanded Broadbill Eurylaimus javanicus SSGI ETF 2 4Black-and-yellow Broadbill Eurylaimus ochromalusNT SSGI ETF 1 5 23 11 52

Pittidae: pittasHooded Pitta Pitta sordida TI ETF 2 PBlue-banded Pitta Pitta arquata TI FS 1Black-and-crimson Pitta Pitta ussheriNT TI ETF 2 3Garnet Pitta Pitta granatinaNT TI ETF 5

Vireonidae: shrike-babblers, erpornis, and alliesWhite-bellied Erpornis Erpornis zantholeuca AFGI FS 6 10 1Acanthizidae: Thornbills and alliesGolden-bellied Gerygone Gerygone sulphurea N/I ES P 1 1

Campephagidae: cuckooshrikes, trillers, and minivetsLesser Cuckooshrike Coracina fimbriata AFGI ETF 2 1 3Fiery Minivet Pericrocotus igneusNT AFGI ETF 1 6Scarlet Minivet Pericrocotus flammeus AFGI ETF 1Oriolidae: Old World oriolesDark-throated Oriole Oriolus xanthonotusNT AFGI/F ETF 3 6 9 10 5

Genera Incertae Sedis: woodshrikes, flycatcher-shrikes, and PhilentomasLarge Woodshrike Tephrodornis gularis AFGI ETF 1Black-winged Flycatcher-shrike Hemipus hirundinaceus SI ETF 3 1 6 2 PRufous-winged Philentoma Philentoma pyrhopterum SI FS 2 1 2 2 5 2Maroon-breasted Philentoma Philentoma velatumNT SI FS 1






2y 5y 7y 2y 5y 7y

Aegithinidae: iorasGreen Iora Aegithina viridissimaNT AFGI ETF 1 8 9 1 13 3

Rhipiduridae: fantailsPied Fantail Rhipidura javanica SI ES 44 44 46 1 9 3 7 8Spotted Fantail Rhipidura perlata SI FS 5

MonarchidaeBlack-naped Monarch Hypothymis azurea SI ETF 1 17 20 26 3 9 21 11Asian Paradise-Flycatcher Terpsiphone paradisi SI ETF 1 2 5 1 3 5 45

Dicruridae: drongosBronzed Drongo Dicrurus aeneus SSGI ETF PGreater Racket-tailed Drongo Dicrurus paradiseus SSGI ETF 2 14

Corvidae: crows, jays, magpies, and treepiesSlender-billed Crow Corvus enca AFGIF OS 6 17 9 29 7 4 7Bornean Black Magpie Platysmurus aterrimusNT AFGIF FS P

Pityriaseidae: bristleheadBornean Bristlehead Pityriasis gymnocephalaNT AFGI FS 1 P

Nectariniidae: sunbirds and spiderhuntersPlain Sunbird Anthreptes simplex NIF ETF P 4 28 1 PBrown-throated Sunbird Anthreptes malacensis NIF OS 1 1 1 11 1 6 4Red-throated Sunbird Anthreptes rhodolaemaNT NI ES 4 P 6Ruby-cheeked Sunbird Anthreptes singalensis NI ES 2 3 11 27Van Hasselt’s Sunbird Leptocoma brasiliana NI ETF P 5 6Olive-backed Sunbird Cinnyris jugularis NI OS 2Crimson Sunbird Aethopyga siparaja NI G 13 12 18 19 5 PTemminck’s Sunbird Aethopyga temminckii NI G PPurple-naped Sunbird Hypogramma hypogrammicum NIF ETF 2 5 6 10 8 28Little Spiderhunter Arachnothera longirostra NI G 20 38 48 13 41 102 98 84Thick-billed Spiderhunter Arachnothera crassirostris NI ETF 1 3Long-billed Spiderhunter Arachnothera robusta NI ETF 1 1Spectacled Spiderhunter Arachnothera flavigaster NIF ETF 2 4 P

Dicaeidae: flowerpeckersYellow-breasted Flowerpecker Prionochilus maculatus AFGI/F ETF 2 7Yellow-rumped Flowerpecker Prionochilus xanthopygius NIF G 14 12 39 37 5 1 21Scarlet-breasted Flowerpecker Prionochilus thoracicusNT NIF ETF POrange-bellied Flowerpecker Dicaeum trigonostigma NIF G 11 25 40 15 3 12 5 37Plain Flowerpecker Dicaeum concolor NIF ETF 1 1 1 P

Chloropseidae: leafbirdsGreater Green Leafbird Chloropsis sonnerati NIF ETF 4 1 18 1 PLesser Green Leafbird Chloropsis cyanopogonNT NIF ETF 1 5

Irenidae: fairy bluebirdsAsian Fairy-bluebird Irena puella AF ES 21 4 6 26Sittidae: NuthatchesVelvet-fronted Nuthatch Sitta frontalis BGI FS 1

Estrildidae: avadavats, parrotfinches, munias, and alliesDusky Munia Lonchura fuscans TF OS P P 6 6 PChestnut Munia Lonchura atricapilla TF OS 6

Sturnidae: starlings and mynasCommon Hill Myna Gracula religiosa AF G 2 5 3 4 30 40

Muscicapidae: old World flycatchers, chats, forktails, and alliesOriental Magpie-Robin Copsychus saularis AFGI OS 2 2White-rumped Shama Copsychus malabaricus AFGI ETF 3 30 26 10 5 13 12 18Rufous-tailed Shama Trichixos pyrropygaNT AFGI FS 2 P 4White-crowned Forktail Enicurus leschenaulti TI FS 1 1Malaysian Blue Flycatcher Cyornis turcosusNT SI ETF PBornean Blue-Flycatcher Cyornis superbus SI FS PVerditer Flycatcher Eumyias thalassina SI ETF 1Rufous-chested Flycatcher Ficedula dumetoriaNT SI FS PGrey-chested Jungle-Flycatcher Rhinomyias umbratilisNT SSGI FS 1 7 3

Pycnonotidae: bulbulsBlack-headed Bulbul Pycnonotus atriceps AFGIF ES 22 26 14 83 12 37 72 17Black-and-white Bulbul Pycnonotus melanoleucusNT AFGIF FS PGrey-bellied Bulbul Pycnonotus cyaniventrisNT AFGIF ETF 2 PPuff-backed Bulbul Pycnonotus eutilotusNT AFGIF FS PYellow-vented Bulbul Pycnonotus goiavier AFGIF G 231 126 108 90 39 4 3 2Olive-winged Bulbul Pycnonotus plumosus AFGIF ES 9 6






2y 5y 7y 2y 5y 7y

Cream-vented Bulbul Pycnonotus simplex AFGIF ES 1 4 17 8 14 34 50Red-eyed Bulbul Pycnonotus brunneus AFGIF ES 1 19 17 89 34 23 73 16Spectacled Bulbul Pycnonotus erythropthalmos AFGIF ETF 3 30 43 86 5 19 20 73Hook-billed Bulbul Setornis crinigerVU AFGIF ETF PBuff-vented Bulbul Iole olivaceaNT AFGIF ES 27 PHairy-backed Bulbul Tricholestes criniger AFGIF FS 1 1 P 8 2 14Finsch’s Bulbul Alophoixus finschiiNT AFGIF ES 2 PYellow-bellied Bulbul Alophoixus phaeocephalus AFGIF FS PGrey-cheeked Bulbul Alophoixus bres AFGIF FS 1 2Streaked Bulbul Ixos malaccensisNT AFGIF ETF 5 PTimaliidae: BabblersBrown Fulvetta Alcippe brunneicaudaNT AFGIF FS 9 47 10Everett’s White-eye Zosterops everetti AFGI ES 20 52 70Black-throated Babbler Stachyris nigricollisNT AFGI ETF 6 2 7 5 42Grey-headed Babbler Stachyris poliocephala AFGI FS 2Chestnut-winged Babbler Stachyris erythroptera AFGI ETF 6 28 12 41 6 50 75 88Chestnut-rumped Babbler Stachyris maculataNT AFGI ETF 4 2 31 16 49 47 57Chestnut-backed Scimitar-Babbler Pomatorhinus montanus BGI FS 14 PRufous-fronted Babbler Stachyris rufifrons AFGI ETF 1 5 3 28 11 7 6 11Bold-striped Tit-Babbler Macronous bornensis AFGI ES 183 197 153 12 132 48 137 29Fluffy-backed Tit-Babbler Macronous ptilosusNT AFGI ETF 6 32 13 15 42 47 65 86Black-capped Babbler Pellorneum capistratum TI ETF 3 27 25 1 6 12 26Moustached Babbler Malacopteron magnirostre AFGI ETF 1 1 3 1 2 3 22Sooty-capped Babbler Malacopteron affineNT AFGI ETF 3 5 10 13 1 15 33Scaly-crowned Babbler Malacopteron cinereum AFGI FS 3 12 9Rufous-crowned Babbler Malacopteron magnumNT AFGI FS 2 5 4 5 5 9White-chested Babbler Trichastoma rostratumNT TI ES 7 4 8 26 68Ferruginous Babbler Trichastoma bicolor AFGI FS 3 6 4 3 11 23Short-tailed Babbler Malacocincla malaccensisNT TI ETF 3 24 11 16 33 17 60

Cisticolidae: cisticolas, tailorbirds, prinias, and alliesAshy Tailorbird Orthotomus ruficeps AFGI ES 69 69 50 25 29 17 28 4Rufous-tailed Tailorbird Orthotomus sericeus AFGI ES 87 159 175 11 49 130 181 7Dark-necked Tailorbird Orthotomus atrogularis AFGI ES 1 2 6 17 59Yellow-bellied Prinia Prinia flaviventris AFGI OS 90 27 12 3 28 6 8 10a Classification follows Myers (2009).b Abbreviations at the ends of names indicate conservation status (www.birdlife.org): VU, vulnerable; NT, near threatened.c Feeding guilds are based on Lambert (1992): R, raptor; NP, nocturnal predator; MP, miscellaneous predator; TI, terrestrial insectivore; AFGI, arboreal foliage glean-

ing insectivore; BGI, bark gleaning insectivore; SSGI, sallying substrate gleaning insectivore; SI, sallying insectivore; AI, aerial insectivore; AFGIF, arboreal foliagegleaning insectivore–frugivore; AFP, arboreal frugivore–predator; SI, sallying insectivore; AI, aerial insectivore; TIF, terrestrial insectivore–frugivore; MIP, miscellaneousinsectivore–piscivore.

d Species were assigned to habitats defined by Rotenberg (2007) and determined according to Sheldon et al. (2001).e “P” indicates species known to occur in a particular forest type but not detected during surveys.

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