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Forest Ecology and Management 261 (2011) 531–544

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Forest Ecology and Management

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

Alison R. Styring a,1, Roslina Ragai b,2, Joanes Unggang b,2, Robert Stuebing b,3, Peter A. Hosner c,4, Frederick H. Sheldon c,∗ a The Evergreen State College, Olympia, WA 98505, United States b Grand Perfect Sdn. Bhd., ParkCity Commerce Square, 97000 Bintulu, Sarawak, Malaysia c Museum of Natural Science, Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, United States article info abstract

Article history: Plantations of exotic trees for industrial and agricultural purposes are burgeoning in the tropics, and Received 24 June 2010 some of them offer the opportunity to study community ecology of animals in a simplified forest set- Received in revised form 1 November 2010 ting. We examined bird community assembly in different aged groves of the industrial tree mangium Accepted 2 November 2010 (Acacia mangium) at two plantations in Malaysian Borneo: Sabah Softwoods near Tawau, Sabah, and Available online 30 November 2010 the 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 into Key words: a secondary forest consisting of a wide diversity of understory trees and shrubs. The bird community Acacia mangium Chronosequence correspondingly increased in species richness and diversity, and we were able to relate these increases Logged forest specifically to canopy height, secondary canopy development, and shrub cover. Species of common, small Mangium bodied frugivores, nectarivores, and insectivores were diverse in older plantation groves, as were com- Sabah mon mid-sized insectivores. However, large, specialized, and normally uncommon taxa (e.g., galliforms, Sarawak pigeons, hornbills, barbets, midsized woodpeckers, muscicapine flycatchers, and wren babblers) were Succession rare or nonexistent in the plantations. Because we lacked species-specific data on foraging, nesting, and other 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 their simple structure, variably aged groves, and bird community richness, are good places to gather such data.

1. Introduction tions is also burgeoning (Barlow et al., 2007; Rotenberg, 2007; Koh, 2008; Sheldon et al., 2010). However, most of these studies have “Industrial” plantations that produce fast growing trees for pulp, focused on determining which kinds of animals occur in planta- composite board, and solid wood products are burgeoning in the tions. Relatively few have taken advantage of plantation structure tropics worldwide (Cossalter and Pye-Smith, 2003; Dvorak, 2004; to study animal ecology, especially community succession. This is Evans, 2009). Because of concern that monocultures of exotic trees surprising because some types of plantations offer a natural exper- will have an adverse effect on biodiversity (Fitzherbert et al., 2008; iment in community assembly. The occurrence of different aged Sodhi et al., 2008), research on native animals in tropical planta- groves of trees at a single location allows the examination of a variety of seral stages at a single point in time and space (e.g., Atkeson and Johnson, 1979; Mitra and Sheldon, 1993; Hanowski et al., 1997; Koh, 2008). This “space-for-time” approach, and the ∗ Corresponding author at: Louisiana State University, Museum of Natural Science, resulting “chronosequence” of observations (Pickett, 1989), allows 119 Foster Hall, Baton Rouge, LA 70808, United States. Tel.: +1 225 578 2887; biologists to compare habitat and community characteristics of col- fax: +1 225 578 3075. E-mail addresses: [email protected] (A.R. Styring), [email protected] onizing species, as long as a plantation’s groves develop adequate (R. Ragai), junis [email protected] (J. Unggang), [email protected] (R. Stuebing), botanical complexity during their relatively short existence. Indus- [email protected] (P.A. Hosner), [email protected] (F.H. Sheldon). trial tree plantations in the tropics are often well suited for such 1 Tel.: +1 360 867 6837; fax: +1 360 867 5430. studies because they comprise extremely fast growing trees that 2 Tel.: +62 086 335880; fax: +62 086 335890. can develop rich secondary understories (Mitra and Sheldon, 1993). 3 Tel.: +62 541 732898; fax: +62 541 732537. 4 Tel.: +1 785 864 3657; fax: +1 785 864 5335. Agricultural plantations, such as oil palm (Elaeis guineensis), how-

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 more We studied bird community development at two industrial tree intensively managed and, thus, unusually depauperate in botanical plantations in Malaysian Borneo. The first was Sabah Softwoods and animal community structure (Koh, 2008; Sheldon et al., 2010). Sdn. Bhd. (hereafter SS). This plantation is located ca. 50 km NNW As long as investigators recognize that seral studies in plantations of Tawau in the Tawau District of southeastern Sabah (Fig. 1) and offer a simplified view of complicated processes, such studies have is administered from Brumas Camp (4◦30N, 117◦E; ca. 300 m ele- the potential to provide insight into important ecological questions, vation). SS was established in 1974 and covers about 60,000 ha, of especially how so many species are able to coexist in tropical rain- which some 35,000–40,000 ha are planted with exotic trees includ- forest (Klopfer and MacArthur, 1961; Karr, 1971). Moreover, such ing mangium (Acacia mangium), Albizia (Paraserianthes falcataria), studies should benefit conservation efforts by providing develop- white teak (Gmelina arborea), and oil palm (E. guineensis)(Pinso ers with information on community ecology that can be translated and Vun, 2000). Several faunal studies have been conducted at SS into plantation design and management to encourage biodiversity (e.g., Duff et al., 1984; Stuebing and Gasis, 1989; Mitra and Sheldon, (Hanowski et al., 1997; Stuebing, 2007; Nasi et al., 2008). 1993; Sheldon et al., 2010), and lists of birds found in native forest at In ornithology, most efforts to understand rainforest bird com- that site have been compiled periodically since 1977 (Sheldon et al., munity succession have focused on chronosequences in natural 2001). The second plantation is the Sarawak Planted Forest Project forest (Terborgh, 1985), logged or burned forests of different ages (hereafter PFP), located ca. 30 km S of Bintulu in the Tatau District of (e.g., Lambert, 1992; Johns, 1996; Barlow and Peres, 2004; Styring central Sarawak (Fig. 1). Its administrative center is the Samarakan and Zakaria, 2004a), or forest recovering from slash-and-burn agri- Nursery (2◦56N, 113◦07E; ca. 50 m elevation). The PFP was estab- culture (e.g., Bowman et al., 1990; Blankespoor, 1991; Raman lished in the mid-1990s, when the Sarawak government set aside et al., 1998; Borges, 2007). The potential for insight from these some 500,000 ha for forest development projects. About 200,000 ha approaches is substantial because each examines change or recov- have been planted with mangium (Stuebing, 2005). Like SS, the PFP ery of native forest, and native forest is richer than exotic forest in has been the focus of several faunal studies (e.g., Stuebing et al., compositional and structural information. This is particularly true 2007; Shadbolt and Ragai, 2010), and lists of birds in the PFP have of studies of natural forest and slash-and-burn succession because been compiled continuously since January 2005 (Stuebing, 2007). chronosequences may span hundreds of years. However, working The groves we examined for this study comprised logged with native systems is difficult. There may be uncertainty about native forest and three age-groups of mangium. Our surveys were the age and sequence of seral stages, or a lack of replicate plots designed to estimate bird species richness (number of species), of the same age, or unclear borders between age groups. Research diversity (number of species adjusted for abundance of individuals in natural forest is particularly difficult because it requires a huge in each), and density (individuals/hectare) occurring in each grove investment of time to understand the terrain and birds (Terborgh, type. Because we expected bird and plant community complex- 1985; Terborgh et al., 1990). Forest recovering from human pertur- ity to be correlated (MacArthur and MacArthur, 1961; Roth, 1976; bation has the additional problem that plots may have experienced Hanowski et al., 1997; Rotenberg, 2007), we related bird occur- different forms and intensity of disturbance (Johns, 1997; Raman rence in each grove to the physical structure of the grove, including et al., 1998). Although studies of bird community succession in its canopy height and cover and the extent of its understory. Bird plantations are limited in scope and reality relative to those in communities occurring in logged native forest patches within the native forest, they still provide information on habitat differences plantations served as points of reference as we assessed several that influence the occurrence and distribution of birds. measures of community structure across plantation age and looked Author's personal copy

A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 533 for overarching patterns. Our fundamental goals were to determine observed, (2) movement of the target organism is not in response which species are early colonizers and which are late, and to assess to movement of the observer, and (3) distances are measured the relationship between species composition and microhabitat. accurately (Thomas et al., 2002). Our surveys were designed to Eventually, with further study of foraging and food, the main goal meet these assumptions. We approached each point quietly and will be to evaluate how morphologically similar, sympatric con- waited several minutes before conducting counts. This allowed geners coexist in Bornean rainforest. any 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 where 2. Methods an individual was located, we made every effort to ensure precise and accurate measurements by mapping and measuring significant Surveys at SS were conducted from 23 June to 12 July 2005 in landscape and habitat features near the point prior to the survey, four grove (or habitat) types: logged native forest, and 2-year-old, mapping bird locations in relation to those features during the sur- 5-year-old, and 7-year-old mangium. Surveys in the PFP were con- vey, and periodic ground-truthing to ensure measurements with ducted from 19 July to 9 August 2006 in the same four habitats. The our rangefinders were accurate. In dense vegetation, it was diffi- logged native forest at SS was located on hills within the plantation cult to say with 100% confidence that all individuals at distance that were too steep for silviculture. This forest was logged lightly in zero were detected, but observers were trained to focus atten- the 1980s and again in the 1990s, thus it exemplified upland section on and near point zero during the survey. Encounter rates ondary forest. The logged native forest in the PFP was retained by were estimated from individual points and detection probability plantation developers as a buffer for the benefit of wildlife. The sec- was modeled and estimated by habitat type and site. Encounter tion we surveyed is the “Bukit Mina Conservation Corridor” (Fig. 1). rates, detection probability and density estimates were calculated It had been logged selectively multiple times since the 1970s and, by habitat. We selected the half-normal key function with a cosine prior to that, was subject to shifting cultivation. It now consists expansion. Cosine adjustments were made sequentially and eval- mainly of old, lowland secondary riverine forest, running in a ca. uated using Aikake’s Information Criterion (AIC) (Thomas et al., 1 km wide strip across the center of part of the plantation. 2010). Point counts were conducted in both plantations along tran- Because of the theoretical expectation that biomass should sects using distance sampling (Buckland et al., 2001). Transects increase with forest maturity (Odum, 1969), we examined the were randomly situated in each habitat type (Fig. 1). Each transect relationship between forest type and mass of its bird community. was 1000 m long and consisted of 20 points, each 50 m apart. Points The average mass of most bird species was computed from Sabah were spaced relatively closely together to provide a comprehensive specimens at the Western Foundation of Vertebrate Zoology, Los inventory. A three-minute bird survey was conducted and habitat Angeles, California (Sheldon et al., 2001). For a few species (<10), data were collected at each point. Characteristics of SS mangium mass was estimated from information in the Handbook of Birds of and logged forest are provided in Sheldon et al. (2010). The number the World or on-line sources. We compared masses between SS and of transects varied among habitat types: 5–6 transects in different PFP and among habitats within each plantation using T-tests and ages of mangium, 6 transects in logged forest at SS, and 12 tran- one-way ANOVA (using JMP), with post hoc comparisons using sects in logged forest at PFP (Appendix A). The close spacing of Tukey–Kramer’s HSD. Because the data were strongly skewed, points, while effective for estimating richness, increased the prob- such that large species were orders of magnitude heavier than the ability of double counting individuals of common species. Before median-sized species, the data were log transformed. This reduced analyzing the data, therefore, we ran summary statistics on detec- skewness significantly, but some very large species still influenced tion distances using R 2.7.2 (Murdoch, 2008). The optimal distance the data. Therefore, in addition to running ANOVA on the log- between points was determined by establishing the 95% detection transformed data, we computed an equivalent non-parametric test radius around each point. We then selected one of the 20 points in (Kruskall–Wallis) for comparison. a transect using a random number table and spaced other points Nonmetric multidimensional scaling was performed in PC-ord accordingly. Observations were truncated at one half of the point to detect patterns in bird community structure related to habitat spacing interval. This subset of samples and observations formed type. We also conducted a randomization procedure (100 runs) the dataset for all subsequent analyses. to determine the optimal number of dimensions to be used in Species accumulation curves, jackknifed estimates of diversity, the ordination. Data were relativized by maximum to reduce the mean point species richness, and Shannon’s Diversity indices (H) influence of rare species, which can skew ordination results dis- were produced using PC-Ord 5 (McCune and Mefford, 2006). To proportionately (McCune and Mefford, 1999). NMS was performed examine the influence of feeding preference on habitat selection, using Bray–Curtis as the distance metric, 1000 runs with real data, a we divided species into feeding guilds (Appendix B) using the classi- stability criterion of 0.0005, and 500 maximum iterations (509 was fication presented in Lambert (1992) and modified by Sheldon et al. the randomly selected start point generated by the analysis). Corre- (2010). To determine the influence of habitat preference on bird lation between individual species and overall community structure distribution, we also classified species by habitat using the groups was determined using Pearson’s correlation coefficients. Correla- defined by Rotenberg (2007) and information on habitat preference tions with an r-squared value greater than 0.20 on any one of the from Lambert (1992) and Sheldon et al. (2001). The groups were: first two axes were considered significant and were plotted onto the FS, forest specialists; ETF, edge tolerant forest specialists; ES, edge ordination as an overlay. A multiple response permutation proce- specialists; OS, open country species; G, generalists; and O, other. dure (MRPP) was also performed in PC-ord to determine variation Mosaic plots were then constructed with JMP 7.0.2 (SAS, 2008)to in bird community composition among habitat types. compare distributions of feeding guilds and habitat types across different groves types. We estimated bird density within each habitat type at each 3. Results site using Distance 6.0 (Thomas et al., 2006). Distance derives its estimates from a detection function of measured distances (radial We conducted 985 point counts of birds and surveys of habitat distance in the case of point counts) of individual birds from the at SS and PFP (455 and 530, respectively) and recorded a total of 111 observer. The estimates are accurate and robust if the follow- bird species (Appendix B). Because our ability to detect individual ing assumptions are met: (1) all individuals at distance zero are birds differed among habitats, we established point-spacing based Author's personal copy

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

Table 1 Sampling and detection statistics.

Plantation Habitat Initial sampling 95% detection Subsequent Resulting sampling effort (no. points) radius (m) spacing of points effort (no. points)

Sabah Softwoods 2-y mangium 99 70 150 35 5-y mangium 119 75 150 36 7-y mangium 120 81.2 200 30 Logged forest 117 88.8 200 29

Sarawak PFP 2-y mangium 88 106.6 250 18 5-y mangium 100 106.6 250 20 7-y mangium 120 91 200 30 Logged forest 222 127 300 32 on bird detectability (Table 1). This resulted in the use of points Table 3 between 150 and 300 m apart and a substantial reduction in points Bird density estimates (individuals/hectare) for mangium (Acacia mangium) and logged forest at Sabah Softwoods (SS) and the Sarawak Planted Forest Project (PFP). analyzed compared to points sampled (130 for SS; 100 for PFP). %CV is the coefficient of variation expressed as a percentage, and L 95 and U 95 are By reducing the sample, we minimized the possibility of double- the lower and upper 95% confidence estimates. counting individual birds. Mean %CV L 95 U 95 Species richness, abundance, diversity, mass, and density are summarized in Tables 2 and 3 and Figs. 2 and 3. Bird species 2-y mangium 13.2 12.8 10.3 17.0 5-y mangium 11.9 16.7 8.6 16.5 in mangium increased in richness, abundance, and diversity with 7-y mangium 13.7 11.2 11.0 17.0 increasing age. Per point species richness and diversity was sim- Logged forest 19.9 8.6 16.9 23.6 ilar and even slightly higher in older mangium compared to logged forest. However, overall estimates of species richness and species accumulation rates were much higher in the logged for- indicated that birds in different plantation age-groups did not differ est, indicating a higher species turnover rate between points in significantly in size, but those in logged native forest were larger on logged forest. Bird density and mass did not increase with plan- average than those in mangium (p < 0.05). This was largely due to tation age, but were significantly higher in logged forest compared greater abundance of some very large-bodied birds in logged forest to plantation. For bird mass, ANOVA and Kruskal–Wallis tests (e.g., pheasants, raptors, hornbills, and large woodpeckers). yielded congruent results. Variation in bird mass among habitats The distribution of foraging guilds differed significantly across was significant: ANOVA, F = 21.2, p < 0.0001; Kruskal–Wallis, Chi- habitats: SS Likelihood Ratio Chi-square = 275.1 p < 0.0001 (Fig. 4). square = 53.0, p < 0.0001. Tukey–Kramer’s pairwise comparisons In general, the number of guilds increased with plantation age,

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

Habitat Observed species richness (and Per-point species Per-point Per-point diversity Mass mean (SD), median Jackknifed estimates of richness) richness abundance (H)

2-y mangium 36 (51–63) 4.9 8.0 1.41 21.9 (43.7), 15.4 5-y mangium 53 (72–84) 5.7 8.3 1.59 24.8 (59.1), 15.4 7-y mangium 62 (85–95) 6.6 9.0 1.76 22.8 (48.8), 15.4 Logged forest 92 (120–131) 5.9 9.4 1.54 61.7 (229.1), 19.26

100 Logged Forest 90

70 7-year Acacia 60

species richness 5-year Acacia 50

40 2-year Acacia 30

20 Average cumulative 10

0 0 10 20 30 40 50 60 70 Number of samples

Fig. 2. Species accumulation curves by habitat type. Author's personal copy

A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 535

1.00 OS G

0.75 FS

0.50 ETF

Mass (log) 0.25

0.00 ed Forest 2-year 5-year 7-year

Acacia Acacia Acacia Logg

1 Fig. 5. Mosaic plot of avian microhabitat preferences by habitat. The height of each 2-year Acacia 5-year Acacia7-year Acacia Logged Forest colored section reflects the proportion of individuals in a particular guild in that Age (grouped) habitat. The width of each column reflects sample size. The microhabitat classes (from Rotenberg, 2007) are: gray (ES) edge specialist, black (ETF) edge tolerant for- Fig. 3. One-way comparison of log bird mass by habitat. The center of each diamond est specialist, yellow (FS) forest specialist, blue (G) generalist, and white (OS) open represents the mean and lines at the tips the 95% confidence interval. The bars country species. (For interpretation of the references to color in this figure legend, within and near the tip of each diamond indicate the overlap in means (calculated the reader is referred to the web version of the article.) as mean ± (( 2)/2 × CI/2).

1.00 nectarivore–insectivores (mainly Arachnothera longirostra). The TI two other guilds were relatively large and diverse: arboreal foliage SSGI gleaning insectivores (mainly tailorbirds and a few species of bab- SI blers) and arboreal foliage gleaning insectivore-frugivores (mainly 0.75 NIF bulbuls). Logged forest communities comprised 12–14 guilds. NI These were more evenly distributed than guilds in the plantation; they were no longer dominated by a few species of bulbuls, 0.50 AFGIF tailorbirds, and babblers. Logged forest also featured a substantial increase in sallying substrate-gleaning insectivores, which are large midstory species such as trogons, broadbills, and dron- 0.25 gos. For microhabitat classes, a similar pattern of increasing bird AFGI community complexity was evident: SS Likelihood Ratio Chi- square = 365.7, p < 0.0001 (Fig. 5). Although all habitat types were dominated by birds favoring forest edge, 7-y mangium and espe- 0.00 AF cially logged forest included a more substantial proportion of forest specialists (e.g., Erpornis zantholeuca, Stachyris poliocephala, Mala- Forest 2-year 5-year 7-year Acacia Acacia Acacia copteron cinereum, and Trichastoma bicolor). Logged NMS randomization (Fig. 6) indicated that two dimensions gen- Fig. 4. Mosaic plot of bird feeding guilds by habitat. The height of each colored erated the least stress in the ordination, and the final ordination section reflects the proportion of individuals in a particular guild in that habitat. The width of each column reflects sample size. The main guilds shown here and MRPP reflected a clear differentiation between native forest are: black (AF) arboreal frugivore, gray (AFGI) arboreal foliage gleaning insecti- and plantation (T = −16.0, A = 0.14, p < 0.0001), with native forest vore, blue (AFGIF) arboreal foliage gleaning insectivore–frugivore, light blue (NI) differing significantly from all plantation types (p ≤ 0.00000005). nectarivore–insectivore, red (NIF) nectarivore–insectivore–frugivore, white (SI) sal- Although some overlap occurred among plantation samples, 2- lying insectivore, yellow (SSGI) sallying substrate-gleaning insectivore, and green year-old mangium differed significantly from older plantation (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 reader samples (p < 0.005). The most similar habitats were 5- and 7- is referred to the web version of the article.) year mangium (p = 0.25). Bird community structure was highly correlated with canopy height, secondary canopy height, percent secondary canopy cover, and shrub height. These were key vari- and logged forest had the greatest guild complexity. Two-year ables in distinguishing logged forest communities from younger mangium contained eight foraging guilds, but was overwhelmingly plantation. Species that correlated strongly with the ordination dominated by two: arboreal foliage gleaning insectivores (Prinia fla- (Fig. 7) included those found almost exclusively in native forest viventris, tailorbirds, and Macronous bornensis) and arboreal foliage (Eurylaimus ochromalus, Harpactes kasumba, Megalaima australis, gleaning insectivore/frugivores (mainly bulbuls). The bird commu- and Irena puella), species found primarily in native forest, but nities of 5-y and 7-y mangium included 9–10 guilds, 6 of which also occurring in lower numbers in older plantation (Orthotomus were well represented. Four of these guilds were still dominated atrogularis and Pycnonotus erythropthalmos), species found primar- by just a few species: terrestrial insectivores (mainly Pellorneum ily in plantation (Macronous bornensis and Orthotomus sericeus), capistratum and Malacocincla malaccensis); sallying insectivores and species found primarily in young plantation and less fre- (mainly Rhipidura javanica); nectarivore-insectivore–frugivores quently in older plantation (Pycnonotus goiavier and Rhipidura (mainly Prionochilus xanothopygius and Dicaeum trigonostigma); javanica). Author's personal copy

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2-year Acacia 1.2 5-year Acacia 7-year Acacia Logged Forest

0.7 % Shrub cover % Secondary canopy cover Canopy height 0.2 Secondary

Axis 2 canopy height

-0.3

-0.8

-1.3 -1.8 -1.3 -0.8 -0.3 0.2 0.7 Axis 1

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 structure and habitat variables with r-squared values greater than 0.5.

4. Discussion (e.g., Lambert, 1992; Johns, 1996; Styring and Zakaria, 2004a; Peh et al., 2005; Edwards et al., 2009). Competition is more difficult 4.1. Species assembly to measure, but is suggested by seral changes in kinds and pro- portions of congeners or morphologically similar species. Terborgh In his classic paper on forest succession and Amazonian bird (1985) also emphasized the interdependence of habitat-choice diversity, Terborgh (1985) listed key factors that influence habi- factors. Food resources, foraging substrates, competition, microcli- tat choice. These included: microclimate, foraging substrates, food mate, cover, nesting, etc., are all related to habitat complexity (e.g., resources, nesting sites, cover, competition, predators, and para- MacArthur and MacArthur, 1961; Bowman et al., 1990). sites. He noted that three of these factors—foraging substrates, food resources, and competition—play especially important roles and 4.1.1. Foraging substrates can be evaluated more readily than the others. Indeed, foraging We examined some of these habitat-choice factors and detected substrates and food resources are assessed in most comparisons the expected trends: bird diversity was strongly associated with of bird communities because they are easy to visualize and quan- the structural complexity of plantation groves. Structural complex- tify; foraging substrates are defined by habitat structure, and food ity in mangium developed relatively quickly. The fast growing crop resources can be observed indirectly by examining feeding guilds trees established a high canopy that provided space for a substantial

2-year Acacia 1.2 5-year Acacia Megalaima australis(0.126,0.232 ) 7-year Acacia Logged Forest Orthotomus atrogularis Correlated species 0.7 (0.096, 0.227) Eurylaimus ochromalus (0.235,0.213) Harpactes kasumba (0.207, 0.110) 0.2

Orthotomus sericeus (0.462,0.026) Axis 2 Pycnonotus erythropthalmos Irena puella (0.329,0.055) Macronous bornensis (0.27, 0.00) (0.587,0.091) -0.3 Rhipidura javanica (0.322,0.093) Pycnonotus goiavier -0.8 (0.254,0.306 )

-1.3 -1.8 -1.3 -0.8 -0.3 0.2 0.7 1.2 Axis 1

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 values greater than 0.20) are plotted. Numbers in parentheses are r-squared values for axis 1 and axis 2, respectively. Author's personal copy

A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 537 understory in five years and sometimes even a distinct midstory in white-eye Zosterops everetti. Also, mangium produces seed pods seven years (Sheldon et al., 2010). On the other hand, 2-y mangium once a year that contain small black seeds with oily orange funi- lacked a canopy and featured largely an open, grass and fern under- cles that attract some small frugivores. The flat canopy of mangium story. NMS randomization showed that canopy height, secondary differs from that of native forest in lacking emergents and large canopy height, percent secondary canopy cover, and shrub height figs. Thus, some canopy specialists, especially large frugivores (e.g., were the key variables distinguishing bird communities among pigeons, hornbills, and barbets) were rare in the mangium. Sub- habitats (Fig. 6). Number of feeding guilds (Fig. 4) and forest spe- canopy development (Fig. 6) in 5-y and 7-y mangium attracted cialist species (Fig. 5) increased with time, and guilds became more numerous large bodied foragers: e.g., malkohas (Phaenicophaeus evenly distributed, presumably because the variety and spatial dis- chlorophaeus and P. curvirostris), trogons (Harpactes diardii), a king- tribution of food resources increased as the plantation became fisher (Ceyx rufidorsum), and some broadbills (Calyptomena viridis more forest-like. and Eurylaimus ochromalus). Most of these feed on large arthropods, Such results are largely intuitive and do not explain in any although C. viridis is a frugivore. Like woodpeckers, these species detail what happens in the bird community as the forest matures. were also attracted to nesting opportunities on older groves (e.g., It would be much more satisfying to know what each individ- H. diardii was observed nesting in a hole in a 7-year mangium snag). ual bird species is doing relative to others. However, this is not The more open understory of older groves also permitted occupa- an easy task because so little information exists about the micro- tion by a few flycatchers, e.g., Hypothymis azurea and Terpsiphone habitat requirements and interactions of Bornean forest species. paradise, but most flycatchers eschewed the plantation (Mitra and No quantitative, comparative foraging or nesting studies exist for Sheldon, 1993; Sheldon et al., 2010). The most dramatic increase in the plantation’s most common species: bulbuls, tailorbirds, and species in mangium occurred in response to the development of low babblers. In fact, the only forest group in insular Southeast Asia shrubs and ground cover. Species associated with these substrates for which we have quantitative comparative foraging information, forage by gleaning or thrashing and included the thrush Copsychus other than hornbills (Leighton, 1982), is woodpeckers (Styring and malabaricus and several forest babblers (Stachyris erythoptera, S. Ickes, 2001a; Styring, 2003; Lammertink, 2004; Styring and Zakaria, maculata, Macronous ptilosus, Pellorneum capistratum, Malacocincla 2004b,a). Nevertheless, NMS provided a quantitative assessment of malaccensis, Trichastoma bicolor, and T. rostratum). Most of these seral changes in a few groups of birds as the plantation aged or was species also nest in the plantation (Sheldon et al., 2001; personal replaced by native forest (Fig. 7). observation). Of the ten species that exhibited abundance patterns that were correlated strongly with NMS ordination (Fig. 7), two pairs (O. 4.1.2. Food resources sericeus and O. atrogularis, and P. goiavier and P. erythropthalmos) Without specific knowledge of arthropod communities, we consisted of congeners that replace one another through time. have relied on changes in forest structure and feeding guilds O. sericeus occurred in low numbers in young groves, unusually (Figs. 4 and 6) to suggest increasing food resources for insec- large numbers in older groves, and low numbers in logged forest tivores and omnivores as the plantation ages. For frugivores (Appendix B). O. atrogularis was rare in young plantation, more and nectarivores, we have more information on potential food common in the older groves, and very common in logged forest. sources (e.g., Kuusipalo et al., 1995; Otsamo, 2000; B. Tan, pers. A third species, O. ruficeps, is common in all ages of plantation, but comm.). occurs in lower numbers in logged forest. A total of seven bulbuls Groves of 2-y mangium were essentially fields of grass, ferns, in the genus Pycnonotus were found in both sites. P. goiavier was and some shrubs (mostly Chromolaena odorata) filled with sapling most abundant in young plantation. It was increasingly replaced in mangiums. Bird food was presumably limited largely to insects and older plantation groves by P. simplex and P. erythropthalmos, both seeds, and the bird community was dominated by a few abundant of which were common in logged forest (Appendix B). P. brun- species (Appendix B): especially, the omnivorous bulbul P. goiavier neus and P. atriceps exhibited conflicting patterns between the two and some foliage gleaning insectivores—the babbler M. bornensis plantations, and P. cyaniventris only occurred in logged forest. Two and three warblers, Orthotomus ruficeps, O. sericeus, and P. flaviven- additional pairs of congeners—M. bornensis and M. ptilosus, and R. tris. Granivores (e.g., Lonchura spp.) that would feed on grass seeds javanica and R. perlata–appeared to replace one another through were rare; instead these were mainly exploited by P. goiavier.A time (Appendix B), but only the occurrence of the early colonist (M. few more bird species would be expected in 2-y mangium during bornensis and R. javanica) was significantly correlated with forest December to March, as seasonal rains increase flowering and fruit- type (Fig. 7). ing and migrants visit from mainland Asia. In general, the open Woodpecker occurrence in mangium provided qualitative country avifauna of Borneo is depauperate, as it is in New Guinea insight into the interplay between habitat structure and bird com- (Bowman et al., 1990), contrasting with relative species richness munity assembly. In young plantation, the only woodpeckers that in cleared areas of tropical Africa and the Neotropics, which have occurred in any numbers were small bodied branch-gleaners, more diverse savanna avifaunas. Sasia abnormis and Meiglyptes tristis, and the ant-termite special- In mature mangium, secondary flora that attracted frugivores ist, Micropternus brachyurus (Appendix B). As the plantation aged, and nectarivores became diverse. The midstory of older groves can trunk specialists (e.g., Blythipicus rubiginosus, Picus puniceus, and include more than 60 tree species in some 24 families, including Dryocopus javensis) started to appear, attracted by an increasing many varieties of fruiting trees, such as Vitex pubscens (Verbe- number of dead and insect-infested trees for foraging and by larger, naceae), Alstonia angustiloba (Apocynaceae), Ficus grossularioides soft-wood boles for nest excavation (Wells, 1999; Styring and (Moraceae), Anthocephalus chinensis (Rubiaceae), Trema tormentosa Zakaria, 2004b; Sheldon et al., 2010). Some species that were not (Cannabaceae), Dillenia suffruticosa (Dilleniaceae), and Macaranga recorded in the plantation (e.g., Reinwardtipicus validus and Picus and Mallotus (Euphorbiaceae) (Mitra and Sheldon, 1993; Kuusipalo mentalis) require a combination of foraging and nesting habitat et al., 1995; Otsamo, 2000). Most of these are secondary forest and canopy cover not met in mangium (Styring and Ickes, 2001b; species imported by birds and bats that presumably rest in the Styring and Zakaria, 2004b). plantation canopy (Kuusipalo et al., 1995). Some of these trees, A variety of other foraging substrates appeared in older planta- e.g., Trema, Mallotus and Macaranga, provide fruit throughout the tion groves. A distinct, flat canopy developed in 5-y and especially year, thus supporting small-bodied birds fairly continuously. Figs, 7-y mangium, and this was frequented by gleaning insectivores in on the other hand, which are the main food of large frugivores relatively large numbers, e.g., the iora Aegithina viridissima and the in primary forest, have short fruit-production periods, and many Author's personal copy

538 A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 individual fig trees are required to support species that depend 5. Future work on them (Zakaria and Nordin, 1998). Thus, pigeons, hornbills, and barbets cannot feed solely within mangium and, with the excep- Future work on birds in Southeast Asian industrial tree plan- tion of the terrestrial dove Chalcophaps indica, were rare in the tations needs to emphasize two kinds of studies: (1) comparative plantation. There were also numerous fruiting and nectar-bearing ecology of species in potentially competing groups (especially bul- shrubs in the plantation, including: Plagiostachys, Hornstedtia buls, babblers, and tailorbirds), and (2) landscape comparisons that scyphifera, and Etlingera (Zingiberaceae); Knema (Myristicaceae); examine the mutual influence of adjacent plantation and native Schumannianthus monophyllus and Stachyphrynium (Marantaceae); forest communities. Community studies need to collect compara- Gardenia sp. (Rubiaceae); Tacca integrifolia (Dioscoreaceae), tive data on foraging, food, nesting, and interspecific interaction. Helminthostachys zeylanica (Ophioglossaceae); and Litsea sp. (Lau- The simple structure of plantation forests and limited numbers of raceae). The gingers and Tacca are well documented as feeding bird species should make it relatively easy to detect more precisely plants for nectarivores, and Knema and Litsea produce fruits eaten the needs of potentially competing taxa. Landscape effects are by hornbills and presumably many other frugivores (Sakai et al., especially important to understanding community assembly and 1999; besgroup.talfrynature.com). improving conservation planning (Renjifo, 2001; Pearman, 2002; Although the connection between the proliferation of fruit- Luck and Daily, 2003; Barlow and Peres, 2004; Edwards et al., bearing trees and frugivores is clear (Fig. 4), the complexities 2010). Communities in adjacent habitats influence one another of interaction are not. Particular bird species cannot be linked in both directions, either from the native forest into plantation to specific fruit because most fruiting trees attract multiple bird (Raman, 2006; Koh, 2008; Sheldon et al., 2010) or vice versa (Ickes species and the interaction of birds and trees is largely proba- et al., 2005). In this study, we attempted to minimize landscape bilistic. However, we detected species changes in the frugivore effects by positioning transects as far as possible from adjacent community (Fig. 7, Appendix B). For example, the generalist P. habitats, and by comparing two plantations that occupied differ- goiavier was continuously replaced through time by an increas- ent locations (550 km apart) and landscapes (PFP in flat lowlands ing number of bulbul species and other medium-sized frugivores, at ca. 50 m in elevation versus SS in rolling uplands at ca. 300 m). e.g., C. viridis, Gracula religiosa, Pycnonotus atriceps, P. brun- Nevertheless, landscape influence is pervasive and important to neus, P. simplex, and P. erythropthalmos. A similar increase in plantation-development planning. nectarivore diversity occurred. In the young plantation the dom- inant species were the sunbirds Anthreptes malaccensis, Aethopyga Acknowledgments siparaja and Arachnothera longirostra and the flowerpeckers Pri- onochilus xanthopygius and Dicaeum trigonostigma. These species We thank the Planted Forest Project, Grand Perfect Sdn. Bhd., increased in abundance as the plantation aged and were joined and Sabah Softwoods Sdn. Bhd. for their kind hospitality and exten- by other nectarivores: e.g., Anthreptes rhodolaema, A. singalensis, sive logistical support of our research. We particularly thank: at Leptocoma brasiliana, Hypogramma hypogrammicum, and Dicaeum Sabah Softwoods Mohd. Hatta Jaafar, Elizabeth Bacamenta, Man- concolor. suit Gamallang, Allison Kabi, Mustapha Pai, and George Tham; and at the Sarawak Planted Forest Project Tony Chaong, Robert 4.2. Biomass Derong, Belden Giman, Last Gundie, Diana James, Azizan Juhin, Joseph Li, Nyegang Megom, Henry Nyegang, Steven Stone, Jimmy In theory, biomass of individual species should increase with Teo, and Latiffah Waini. For technical advice on plants, we thank forest age, as selective advantage shifts to larger organisms that Dr. Benito Tan, Paul Leong, and Serena Lee of the Herbarium of have more complex life histories and which live longer in the the Singapore Botanical Gardens. Permission to undertake research relatively stable environment of mature forest (Odum, 1969). How- in Sabah was provided by the Malaysian Economic Planning Unit ever, this expected pattern is not always found empirically (Bock of the Prime Minister’s Department, and help with research in and Lynch, 1970; Helle, 1985). We did not detect a size change the State has been continuously aided by Sabah Wildlife Depart- as the plantation age, probably because the amount of time (7 ment (Datuk Mahedi Andau, Laurentius Ambu, Augustine Tuuga, years) was inadequate for a substantial change to develop. We and Peter Malim), Sabah Parks (Datuk Lamri Ali, Dr. Jamili Nais, did find, however, that biomass of individual bird species and and Maklarin Lakim), and Sabah Museum (Datuk Joseph Guntavid, variation in size among species were on average much higher in Jaffit Majuakim, and Albert Lo). Permission to undertake research logged native forest than in exotic tree groves (Fig. 3); the logged in Sarawak was provided by the Sarawak Forestry Department, forest housed not only many small and medium-sized birds, but Sarawak Forestry Corporation, and Sarawak Biodiversity Centre. also unusually large ones, e.g., pheasants, trogons and hornbills. The research was funded by the Coypu Foundation of Louisiana, These differences make sense in light of the greater variation in Disney Worldwide Conservation Fund, Grand Perfect Sdn. Bhd., food and nesting resources in native forest versus the plantation Louisiana State University, Sabah Softwoods Sdn. Bhd, and The (Fig. 6). Evergreen State College. Author's personal copy

A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 539

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 Softwoods 1. AM2Y1 Acacia mangium 2 23-June-05 FHS/PAH 2. AM2Y2 Acacia mangium 2 27-June-05 FHS 3. AM2Y3 Acacia mangium 2 28-June-05 FHS 4. AM2Y4 Acacia mangium 2 5-July-05 FHS 5. AM3Y1 Acacia mangium 2 12-July-05 FHS 6. AM5Y1 Acacia mangium 5 25-June-05 PAH 7. AM5Y2 Acacia mangium 5 29-June-05 PAH 8. AM5Y3 Acacia mangium 5 30-June-05 FHS 9. AM5Y4 Acacia mangium 5 6-July-05 FHS 10. AM5Y5 Acacia mangium 5 10-July-05 FHS 11. AM5Y6 Acacia mangium 5 11-July-05 FHS 12. AM7Y1 Acacia mangium 7 24-June-05 FHS/PAH 13, AM7Y2 Acacia mangium 7 30-June-05 PAH 14. AM7Y3 Acacia mangium 7 7-July-05 PAH 15. AM7Y4 Acacia mangium 7 8-July-05 PAH 16. AM7Y5 Acacia mangium 7 10-July-05 PAH 17. AM7Y6 Acacia mangium 7 12-July-05 PAH 18. LF1 Logged native forest Secondary hill forest 28-June-05 PAH 19. LF2 Logged native forest Secondary hill forest 4-July-05 PAH 20. LF3 Logged native forest Secondary hill forest 5-July-05 PAH 21. LF4 Logged native forest Secondary hill forest 6-July-05 PAH 22. LF5 Logged native forest Secondary hill forest 9-July-05 PAH 23. LF6 Logged native forest Secondary hill forest 9-July-05 FHS

Sarawak Planted Forest Project 1. AM2Y1 Acacia mangium 2 19-July-06 ARS 2. AM2Y2 Acacia mangium 2 28-July-06 FHS 3. AM2Y3 Acacia mangium 2 28-July-06 ARS 4. AM2Y4 Acacia mangium 2 29-July-06 FHS 5. AM2Y5 Acacia mangium 2 29-July-06 ARS 6. AM5Y1 Acacia mangium 5 20-July-06 ARS 7. AM5Y2 Acacia mangium 5 30-July-06 FHS 8. AM5Y3 Acacia mangium 5 30-July-06 ARS 9. AM5Y4 Acacia mangium 5 1-August-06 FHS 10. AM5Y5 Acacia mangium 5 1-August-06 ARS 11. AM7Y1 Acacia mangium 7 26-July-06 FHS 12. AM7Y2 Acacia mangium 7 26-July-06 ARS 13. AM7Y3 Acacia mangium 7 27-July-06 FHS 14. AM7Y4 Acacia mangium 7 27-July-06 ARS 15. AM7Y5 Acacia mangium 7 31-July-06 FHS 16. AM7Y6 Acacia mangium 7 31-July-06 ARS 17. LF A1 Logged native forest Secondary riverine forest 21-July-06 ARS 18. LF A2 Logged native forest Secondary riverine forest 22-July-06 ARS 19. LF A3 Logged native forest Secondary riverine forest 23-July-06 ARS/FHS 20. LF A4 Logged native forest Secondary riverine forest 24-July-06 ARS 21. LF A5 Logged native forest Secondary riverine forest 25-July-06 ARS 22. LF A6 Logged native forest Secondary riverine forest 24-July-06 FHS 23. LF B1 Logged native forest Secondary riverine forest 3-August-06 FHS 24. LF B2 Logged native forest Secondary riverine forest 3-August-06 ARS 25. LF B3 Logged native forest Secondary riverine forest 4-August-06 FHS 26. LF B4 Logged native forest Secondary riverine forest 4-August-06 ARS 27. LF B5 Logged native forest Secondary riverine forest 5-August-06 FHS 28. LF B6 Logged native forest Secondary riverine forest 5-August-06 ARS Author's personal copy

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

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 pheasants Scaly-breasted Partridge Arborophila charltoniiNT TIF FS 2 6 Crested Fireback Lophura ignitaNT TIF FS 4 P Great Argus Argusianus argusNT TIF FS 1 10 3

Accipitridae: hawks, eagles, and allies Jerdon’s Baza Aviceda jerdoni RESP 2P Oriental Honey-buzzard Pernis ptilorhynchus RESP 12 P Bat Hawk Macheiramphus alcinus ROS 2 Brahminy Kite Haliastur indus ROS P Lesser Fish-Eagle Ichthyophaga humilisNT ROS P Crested Serpent-Eagle Spilornis cheela RG 131 438 Black Eagle Ictinaetus malayensis ROS 1 Changeable Hawk-Eagle Spizaetus cirrhatus RG 1

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

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

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

Strigidae: typical owls Reddish Scops Owl Otus rufescensNT NP FS P Sunda Scops Owl Otus lempiji NP FS P Barred Eagle Owl Bubo sumatranus NP ETF P Buffy Fish Owl Ketupa ketupu NP ES P Brown Wood Owl Strix leptogrammica NP FS P Brown Boobook Ninox scutulata NP FS P

Podargidae: frogmouths Gould’s Frogmouth Batrachostomus stellatusNT SSGI FS P

Caprimulgidae: nightjars Malaysian Eared Nightjar Eurostopodus temminckii AI OS 3

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

Trogoniformes: Trogonidae Red-naped Trogon Harpactes kasumbaNT SSGI FS 1 8 2 42 Diard’s Trogon Harpactes diardiiNT SSGI FS 1 1 2 5 8 10 Author's personal copy

A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 541

Appendix B. (Continued)

Namesa Guildc Habitatd 2005 Survey SSe 2006 Survey PFPe

English Scientiﬁcb Acacia LNF Acacia LNF

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

Cinnamon-rumped Trogon Harpactes orrhophaeusNT SSGI FS P Scarlet-rumped Trogon Harpactes duvauceliiNT SSGI FS 1 12 1 2 2 Coraciidae: Rollers Dollarbird Eurystomus orientalis SI OS P P

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

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

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

Indicatoridae: honeyguides Malaysian Honeyguide Indicator archipelagicusNT MI/P FS P

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

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

Pittidae: pittas Hooded Pitta Pitta sordida TI ETF 2 P Blue-banded Pitta Pitta arquata TI FS 1 Black-and-crimson Pitta Pitta ussheriNT TI ETF 2 3 Garnet Pitta Pitta granatinaNT TI ETF 5

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

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

Genera Incertae Sedis: woodshrikes, ﬂycatcher-shrikes, and Philentomas Large Woodshrike Tephrodornis gularis AFGI ETF 1 Black-winged Flycatcher-shrike Hemipus hirundinaceus SI ETF 3 1 6 2 P Rufous-winged Philentoma Philentoma pyrhopterum SI FS 2 1 2 2 5 2 Maroon-breasted Philentoma Philentoma velatumNT SI FS 1 Author's personal copy

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

Appendix B. (Continued)

Namesa Guildc Habitatd 2005 Survey SSe 2006 Survey PFPe

English Scientiﬁcb Acacia LNF Acacia LNF

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

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

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

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

Dicruridae: drongos Bronzed Drongo Dicrurus aeneus SSGI ETF P Greater Racket-tailed Drongo Dicrurus paradiseus SSGI ETF 2 14

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

Pityriaseidae: bristlehead Bornean Bristlehead Pityriasis gymnocephalaNT AFGI FS 1 P

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

Dicaeidae: ﬂowerpeckers Yellow-breasted Flowerpecker Prionochilus maculatus AFGI/F ETF 2 7 Yellow-rumped Flowerpecker Prionochilus xanthopygius NIFG 14123937 5 121 Scarlet-breasted Flowerpecker Prionochilus thoracicusNT NIF ETF P Orange-bellied Flowerpecker Dicaeum trigonostigma NIF G 11 25 40 15 3 12 5 37 Plain Flowerpecker Dicaeum concolor NIF ETF 1 1 1 P

Chloropseidae: leafbirds Greater Green Leafbird Chloropsis sonnerati NIF ETF 4 1 18 1 P Lesser Green Leafbird Chloropsis cyanopogonNT NIF ETF 1 5

Irenidae: fairy bluebirds Asian Fairy-bluebird Irena puella AF ES 21 4 6 26 Sittidae: Nuthatches Velvet-fronted Nuthatch Sitta frontalis BGI FS 1

Estrildidae: avadavats, parrotﬁnches, munias, and allies Dusky Munia Lonchura fuscans TF OS P P 6 6 P Chestnut Munia Lonchura atricapilla TF OS 6

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

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

Pycnonotidae: bulbuls Black-headed Bulbul Pycnonotus atriceps AFGIF ES 22 26 14 83 12 37 72 17 Black-and-white Bulbul Pycnonotus melanoleucusNT AFGIF FS P Grey-bellied Bulbul Pycnonotus cyaniventrisNT AFGIF ETF 2 P Puff-backed Bulbul Pycnonotus eutilotusNT AFGIF FS P Yellow-vented Bulbul Pycnonotus goiavier AFGIF G 231 126 108 90 39 4 3 2 Olive-winged Bulbul Pycnonotus plumosus AFGIF ES 9 6 Author's personal copy

A.R. Styring et al. / Forest Ecology and Management 261 (2011) 531–544 543

Appendix B. (Continued)

Namesa Guildc Habitatd 2005 Survey SSe 2006 Survey PFPe

English Scientiﬁcb Acacia LNF Acacia LNF

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

Cream-vented Bulbul Pycnonotus simplex AFGIF ES 1 4 17 8 14 34 50 Red-eyed Bulbul Pycnonotus brunneus AFGIF ES 1 19 17 89 34 23 73 16 Spectacled Bulbul Pycnonotus erythropthalmos AFGIF ETF 3 30 43 86 5 19 20 73 Hook-billed Bulbul Setornis crinigerVU AFGIF ETF P Buff-vented Bulbul Iole olivaceaNT AFGIF ES 27 P Hairy-backed Bulbul Tricholestes criniger AFGIF FS 1 1 P 8 2 14 Finsch’s Bulbul Alophoixus finschiiNT AFGIF ES 2 P Yellow-bellied Bulbul Alophoixus phaeocephalus AFGIF FS P Grey-cheeked Bulbul Alophoixus bres AFGIF FS 1 2 Streaked Bulbul Ixos malaccensisNT AFGIF ETF 5 P Timaliidae: Babblers Brown Fulvetta Alcippe brunneicaudaNT AFGIF FS 9 47 10 Everett’s White-eye Zosterops everetti AFGI ES 20 52 70 Black-throated Babbler Stachyris nigricollisNT AFGI ETF 6 2 7 5 42 Grey-headed Babbler Stachyris poliocephala AFGI FS 2 Chestnut-winged Babbler Stachyris erythroptera AFGI ETF 6 28 12 41 6 50 75 88 Chestnut-rumped Babbler Stachyris maculataNT AFGI ETF 4 2 31 16 49 47 57 Chestnut-backed Scimitar-Babbler Pomatorhinus montanus BGI FS 14 P Rufous-fronted Babbler Stachyris rufifrons AFGI ETF 15328117611 Bold-striped Tit-Babbler Macronous bornensis AFGI ES 183 197 153 12 132 48 137 29 Fluffy-backed Tit-Babbler Macronous ptilosusNT AFGI ETF 6 32 13 15 42 47 65 86 Black-capped Babbler Pellorneum capistratum TIETF3 27251 6 1226 Moustached Babbler Malacopteron magnirostre AFGI ETF 1 1 3 1 2 3 22 Sooty-capped Babbler Malacopteron affineNT AFGI ETF 3 5 10 13 1 15 33 Scaly-crowned Babbler Malacopteron cinereum AFGI FS 3 12 9 Rufous-crowned Babbler Malacopteron magnumNT AFGI FS 2545 59 White-chested Babbler Trichastoma rostratumNT TI ES 7 4 8 26 68 Ferruginous Babbler Trichastoma bicolor AFGI FS 3 6 4 3 11 23 Short-tailed Babbler Malacocincla malaccensisNT TIETF3 241116 331760

Cisticolidae: cisticolas, tailorbirds, prinias, and allies Ashy Tailorbird Orthotomus ruficeps AFGI ES 69 69 50 25 29 17 28 4 Rufous-tailed Tailorbird Orthotomus sericeus AFGI ES 87 159 175 11 49 130 181 7 Dark-necked Tailorbird Orthotomus atrogularis AFGI ES 1 2 6 17 59 Yellow-bellied Prinia Prinia flaviventris AFGI OS 90 27 12 3 28 6 8 10 a 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 gleaning insectivore; BGI, bark gleaning insectivore; SSGI, sallying substrate gleaning insectivore; SI, sallying insectivore; AI, aerial insectivore; AFGIF, arboreal foliage gleaning insectivore–frugivore; AFP, arboreal frugivore–predator; SI, sallying insectivore; AI, aerial insectivore; TIF, terrestrial insectivore–frugivore; MIP, miscellaneous insectivore–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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