Effects of Forestry Practices on Vegetation Structure and Bird

Biological Conservation 107 (2002) 229–240 www.elsevier.com/locate/biocon

Eﬀects of forestry practices on vegetation structure and bird community of Kibale National Park, Uganda

Cagan H. Sekercioglu* Center for Conservation Biology, Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020, USA

Received 12 September 2001; received in revised form 8 January 2002; accepted 12 February 2002

Abstract I examined the lingering effects of past timber management practices on the vegetation structure and bird community of Kibale National Park, Uganda. I compared four forest treatments: unlogged native forest (UL), two that were selectively logged at low (LL) and high (HL) intensities in the 1960s, and a conifer plantation (PL). Forest-dependent birds were best represented at UL. LL was similar to UL in both vegetation structure and bird community composition, although some forest-dependent bird species were missing from the former. HL had significantly less canopy closure and lower tree density than other plots as a result of the combination of extensive secondary damage and natural disturbance patterns that prevented the reclosure of the forest canopy. Thirty-one percent of the forest-dependent bird species observed during the study were not detected at HL. At PL, bird species richness and bird abundance were about a third of those observed in other plots. There were significant correlations between heterogeneity of tree distribution (horizontal heterogeneity) and abundance and species richness of birds across plots. Abundance and species richness of all, forest-dependent, and forest generalist birds were highest in plots with intermediate measures of horizontal heterogeneity, which were mostly unlogged or lightly logged. If reduced-impact logging practices are not implemented during selective logging operations in tropical forests, consequent long-term changes in vegetation structure may result in significant declines in the populations of some forest-dependent species, as was observed in Kibale National Park. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Uganda; Tropical forestry; Selective logging; Vegetation structure; Bird communities

1. Introduction Basal area, canopy cover, and canopy height are reduced while average gap size and distance between Selective timber extraction is often proposed as a sus- trees increase. The distribution of trees becomes less tainable, low-impact alternative to clear-cut logging, uniform, with gaps separating unlogged patches (Skor- and is the most frequent form of logging in the tropics upa and Kasenene, 1984; Johns, 1985, 1988, 1992; (Repetto and Gillis, 1988; Abramovitz and Matoon, Struhsaker, 1997; Thiollay, 1997). 1999; Anonymous, 2001). However, despite the long- Structural changes in vegetation modify the forest term reductions in ﬁnancial costs and environmental microclimate by altering temperature, humidity, light, damage associated with reduced-impact logging (RIL), and wind levels. Higher temperatures and lower humid- because of the initial costs and lack of governmental ity result in soil desiccation, higher seed mortality, and incentives, training and guidance, most tropical selective lower tree recruitment (Pinard and Putz, 1996). Stimu- logging operations do not employ RIL, and cause high lated by high light levels, rapidly growing shrubs levels of secondary damage (Putz et al., 2000, 2001). frequently become dominant (Struhsaker, 1997). This Even though only 3–10% of the trees in a selectively dense shrub cover attracts seed predators such as logged area are removed for commercial use, 40–80% of rodents and insects (Isibirye-Basuta and Kasenene, the trees are destroyed as a result of the creation 1987; Pinard and Putz, 1996), and herbivores such as of logging tracks, falling trees bringing down neighbor- African elephants (Elephas maximus) and red river hogs ing trees, and heavy activity of forestry machinery. (Potamochoerus porcus; Nummelin, 1990; Struhsaker et al., 1996), which further retard tree regeneration. *Tel.: +1-650-724-6355; fax: +1-650-723-5920. Increased wind breaks branches and fells trees, resulting E-mail address: [email protected] (C.H. Sekercioglu). in a more open forest canopy that promotes the growth

0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(02)00097-6 230 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 of understory shrubs. These changes may persist for only about 5% across all Parinari forest subtypes decades (Thiollay, 1997; Struhsaker, 1997). (Kingston, 1967, in Chapman and Chapman, 1997). I After the wholesale clearance of large areas of tropical will be using the abbrevations UL (unlogged), LL forest in southeast Asia and western Africa, the atten- (lightly logged), HL (heavily logged), and PL (plantation of the international logging community has now tion) for the treatments throughout the paper. turned towards the remaining relatively pristine rain- UL is the least disturbed of the compartments. forests of Latin America and central Africa (Dranzoa, Although it was occasionally logged by pit-sawyers 1995). I investigated the long-term effects of forestry between 1950 and 1970, no commercial, mechanized, practices on the forest bird community and vegetation large-scale logging was done and fewer than three trees structure of a medium altitude Afrotropical forest. My were removed per km2 (Struhsaker, 1997). This is con- objectives were to (1) assess the long-term changes in sidered to be similar to natural treefall rates, with little, the vegetation structure of sites with different timber if any, impact on wildlife (Skorupa and Kasenene, management histories, (2) compare the forest bird com- 1984). Like past researchers (Dranzoa, 1995; Chapman munities of these sites, and (3) investigate whether any and Chapman, 1996, 1997; Struhsaker, 1997), I used measures of vegetation structure correlated with the this ‘‘unlogged’’ site as the forest control treatment. abundance and species richness of forest bird species. Parinari excelsa, Celtis durandii, and Markhamia platy- Two of the sites had been selectively logged (14 and 21– calyx are the dominant trees, and Mimulopsis solmsii 80 m3/ha), one was almost unlogged and the fourth was and Palisota schweinfurthii commonly occur in the a Pinus plantation. understory (Struhsaker, 1997). LL, vegetationally similar to UL, was selectively logged in 1969 at an average rate of 14 m3/ha (about 400 trees/km2) resulting in a tree 2. Methods basal area reduction of 25% (Skorupa and Kasenene, 1984; Struhsaker, 1997). 2.1. Study area HL was selectively logged in 1968–1969. Even though the official estimate of logging for HL is 21 m3/ha, This study was conducted at Kanyawara biological Dranzoa (1998) suggested that the actual logging den- field station of Makarere University, situated in medium sity was much higher, possibly 80 m3/ha or more. The altitude (1530 m) moist evergreen forest of Kibale basal area reduction was 47% (Struhsaker, 1997). National Park (766 km2) in western Uganda (0130N– The most common tree species are Diospyros abyssinica, 0410N and 30190E–30320E; see Struhsaker, 1997, for a Markhamia platycalyx,andCeltis durandii, and there is detailed map). Mean annual rainfall at Kanyawara is dense undergrowth of Acanthus and Mimulopsis spp. approximately 1740 mm, with a dry season between UL, LL, and HL have originally been classified as Par- May and August. Yearly mean temperature is 23.1 C. inari forest, are well matched in their vegetative affi- The forest is a mixture of pure forest stands (60%) and nities, topography, and climate (Skorupa and Kasenene, successional grassland, swamp forests, and secondary 1984; Struhsaker, 1997). forests (Chapman and Chapman, 1996). PL is a Pinus caribbaea/Pinus patula plantation dating from 1963 when trees were planted over elephant grass 2.2. Study sites (Pennisetum purpureum). Although this is not native forest, it is a useful site for the purpose of this study Between June and August 1996, I collected data from since exotic tree plantations often form a part of tropi- 10 plots distributed in approximately 80 ha in each of cal forestry operations to facilitate the reformation of four compartments: unlogged forest (K-30, 282 ha), native forest cover, and PL hosts many colonizing forest lightly logged forest (K-14, 405 ha), heavily logged for- plants utilized by forest birds and mammals (Chapman est (K-15, 347 ha), and an exotic Pinus caribbaea/Pinus and Chapman, 1996). The shrubs Achyranthes aspera, patula plantation (K-34/ Nyakatojo, 400 ha; Struhsaker, Pollia condensate,andPteridium aquilinium as well as 1997). Due to the limitations of the trail grid, I gathered many recolonizing indigenous tree species commonly data from only one compartment for each treatment. occur in the understory. Since September 1993, logging Because the study plots were widely separated, I make operations involving portable sawmills and/or pit- the assumptions that the data obtained is representative sawing have taken place at this site (Chapman and of the vegetation structure and bird community of Chapman, 1996). Kanyawara and that the effects of pseudoreplication were minimal (Oksanen, 2001). The results should be 2.3. Vegetational surveys interpreted in light of these assumptions. The forest at Kanyawara was originally classified as Vegetational structural measurements were conducted Parinari forest and vegetative features such as cumula- as point surveys and included diameter at breast-height tive basal area, canopy cover and stem density vary by (DBH), point-centered quarter measurements of tree C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 231 distance (PQD), percent canopy closure (PCC), and covered one habitat, all surveys took place at least 50 m vertical vegetation distribution (VVD). away from any habitat edges and swampy areas were The locations of point surveys were evenly distributed avoided. All surveys were conducted between 06:30 and across the trail grid in each compartment, with at least 12:00, the time of greatest bird activity. Six bird surveys 50 m between each survey. The surveys were conducted were conducted in each plot, for a total of 60 surveys per at least 10 m away from the trails, which were approxi- treatment. mately 1 m wide on average. Ten surveys were conducted in each plot, for a total of 100 surveys for 2.5. Data analysis each treatment. Percent canopy closure (Jennings et al., 1999) was measured using a convex mirror (type-A 2.5.1. Vegetation structure spherical) densiometer. Densiometer readings in four Since higher habitat structural heterogeneity often directions were averaged for each point. This method increases bird species richness due to the presence of over-estimates canopy closure in areas with a high more diverse nesting and foraging resources (MacAr- understory-to-canopy ratio, such as HL (Kasenene, thur and MacArthur, 1961; Roth, 1976), I calculated 1987, in Dranzoa, 1995). indices of horizontal heterogeneity of vegetation (IHH) To measure vertical vegetation structure, I used a and vertical heterogeneity of vegetation (IVH). IVH is clinometer and a 3-m measuring stick to estimate the Shannon–Wiener index for vertical vegetation dis- 0 vegetation presence–absence at 0.5, 1, 2, 3, 5, 10, 15, 20, tributions (H VVD), taking the number of vegetation 25, and 30+ m. Facing north, I placed the stick ver- touches at each height as individuals in that class. I 0 tically on the ground, and checked for vegetation compared the IVH (H VVD) values using the appro- presence within a circle of 5 cm radius at each height priate t-test (Magurran, 1988). IHH (Roth, 1976) is level. For heights >5 m, I looked along the stick up into the coefficient of variation of point-centered quarter the canopy, and estimated each height level. Based on distance (PQD) measurements where: estimates of tree heights that were later measured, height estimations were accurate to approximately IHH ¼ ðÞStandard deviationðÞ PQD =ðÞAverageðÞ PQD Æ6%. When I had a doubt, I measured the height with a clinometer. IHH is lowest if trees are distributed uniformly, At each sampling point, I measured the distance from higher for a random distribution and highest for a clus- the point to the nearest tree with at least 10 cm DBH in tered distribution. each quarter of a hypothetical circle (the point-quarter DBH distribution and vertical vegetation distribution distance, PQD; Roth, 1976). I also measured the DBH were compared between sites using Morisita-Horn index of each tree. of similarity (MHIS; Magurran, 1988) where: X 2.4. Bird surveys MHIS ¼ 2 ni;a Áni;b =ðÞNa ÁNb ÁðÞda þ db

I used the fixed-area survey method of Thiollay (1997), which makes cross-site comparisons possible for i classes (of DBH and vegetation height), ni,a is the and reduces the bias that results from unequal detect- number of measurements in the ith class at site A, ni,b is ability. Even though all the sites surveyed were forested, the number of measurements in the ith class at site B, Na there are bound to be differences in habitat openness, is the total number of measurements at site A, Nb is the which affects bird detectability (Bibby et al., 2000). Like total number of measurements at site B, most bird survey methods, this method is biased against X 2 2 nocturnal species and against quiet and secretive species da ¼ ni;a =Na that do not flush easily (Bibby et al., 2000). The results must be interpreted with these caveats in mind. I use the survey results only as indicators of relative and frequency of occurrence rather than as estimates of X 2 2 absolute density. Each bird survey covered an area db ¼ ni;b =Nb: of 50Â50 m (0.25 ha). Survey areas were distributed evenly, with at least 100 m between areas and at least 200 m between surveys conducted in the same day. For each survey, I covered 50 m in 20 min, noting the pre- 2.5.2. Bird communities sence of any birds seen or heard within 25 m on each Species were assigned to the category of forest- side of transect. I included the birds that I flushed dependent species (FD), forest generalists (FG) and from the survey area. Birds that were flying over or non-forest species (NF), based on Bennun et al. (1997) through the survey area were not counted. Each survey and Dranzoa (1995). Forest-dependent species such as 232 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 crowned hawk-eagle (Sthephanoaetus coronatus) and significantly differ between other treatments (all gray parrot (Psittacus erithracus) do not occur outside w2 <18.81, all P>0.10). At PL, the mode of DBH dis- primary forests and are mainly restricted to forest tribution was 35 cm whereas in other sites it was 10 cm. interior and understory. Forest generalists, such as Vertical vegetational distribution (Table 1) was sig- crested guineafowl (Guttera pucherani) and African nificantly different between treatments (all w2 >30.08; green-pigeon (Treron calva), mainly occur in the all P<0.01) as well, except between UL and LL canopy, edge and treefall gaps of undisturbed forest. (w2=5.29, P>0.25). HL had significantly less vertical They are also frequently found in secondary forest and heterogeneity (IVH) than the rest of the sites (all have higher tolerance of disturbance. Non-forest species t>4.546, all P<0.001). The index of horizontal hetero- such as common bulbul (Pycnonotus barbatus) African geneity, based on PQD values (Table 1), revealed that and yellow white-eye (Zosterops senegalensis) are not PL was the least horizontally heterogeneous treatment, found in forest except in the herbaceous vegetation of whereas HL had the highest horizontal heterogeneity large gaps, as transients and in the conifer plantation. and UL and LL had intermediate values. Birds were also categorized into 13 feeding guilds such MHIS was highest between UL and LL for all vege- as frugivores, bark-gleaning insectivores, granivores, tational measures (Table 2). In terms of vertical dis- etc. based on Dranzoa (1995). I used EstimateS (Col- tribution of vegetation, UL and LL were more similar well, 1997) to estimate richness of all species and species to PL than to HL, whereas the opposite was true for of different forest-dependence classes, using ACE DBH distribution. (Abundance-based coverage estimator), ICE (Incidence- based coverage estimator; Chazdon et al., 1998), Chao1, 3.2. Bird communities Chao2, Jackknife1, Jackknife2, Michaelis-Menten, and Bootstrap methods (Colwell and Coddington, 1994). 3.2.1. Richness I compared the avifaunas of different treatments using One hundred and twenty-eight species were observed Morisita-Horn index of similarity, substituting the total during the study (Fig. 1). HL had the highest numbers number of individuals at site A for Na and the number of individuals and species as a result of the high species of individuals in the ith species at site A for ni,a. richness of forest generalist and non-forest species at this site. However, it should be noted that HL also had the most open vegetation structure, hence best visibility. 3. Results UL had the highest observed and predicted species richness of forest-dependent species. 3.1. Vegetation structure 3.2.2. Similarity HL had significantly less canopy closure (all t>5.23, Non-plantation treatments shared 76–83% of their all P<0.0001, n=100/treatment) than other treatments species and each shared 45–47% of its species with PL. (Table 1), which were not significantly different from When all species were considered, MHIS showed a each other (all t<0.57; all P>0.5). Average DBH dif- similar pattern (Table 3). UL and LL shared 80% of fered significantly among treatments (all t>2.60, all their non-forest species, whereas UL and HL shared P<0.001, n=400/treatment), except between UL and 36%, and LL and HL shared 45%. The MHIS values LL (t=1.71, P=0.087). Average PQD values (Table 1) reflected these differences. were also significantly different between treatments (all t>3.64, all P<0.001, n=400/treatment), except 3.2.3. Abundance and rarity between UL and LL (t=1.75, P=0.08). DBH distribu- A species was considered rare if it made up less than tion was significantly different between PL and the 1% of the total sample. When the proportion of rare other treatments (all w2>88.16, all P<0.01), but did not species to the total number of species in all the surveys

Table 1 Vegetational structural parameters of sites with standard errors

Parameter UL LL HL PL

Average PCC (cm) 91.05Æ0.85 91.56Æ0.78 78.71Æ2.20 91.04Æ0.47 Average PQD (cm) 318.00Æ8.98 296.29Æ8.53 598.10Æ25.17 259.88Æ5.24 Average DBH (cm) 30.70Æ1.15 28.09Æ0.99 23.70Æ0.69 34.04Æ0.56 H0 DBH 2.52 2.37 2.13 2.20 IHH (CV of PQD) 0.58 0.58 0.84 0.40 IVH (H 0 VVD) 2.28 2.29 2.13 2.26

CV, coeﬃcient of variation; DBH, diameter at breast-height; H 0, Shannon’s diversity index; IHH, index of horizontal heterogeneity; PQD, point- quarter distance; PCC, percent canopy closure; VVD, vertical vegetation distribution. C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 233

Table 2 Table 3 Morisita-Horn similarity of diameter-at-breast height (below diag- Morisita-Horn similarity of bird community composition onal) and vertical vegetational distribution (above diagonal) UL LL HL PL UL LL HL PL UL – 76/69 69/49 40/57 UL – 88 57 70 LL 79/75 – 68/68 43/53 LL 80 – 60 72 HL 70/68 71/63 – 48/52 HL 73 79 – 52 PL 45/32 47/28 52/34 – PL 44 39 36 – Values are given for all (below diagonal and left), forest-dependent (below diagonal and right), forest generalist (above diagonal and left), and non-forest (above diagonal and right) species.

P<0.0001 ) for all groups except NF birds (Fig. 3). Bird species richness and abundance at plots reached an asymptote at intermediate values of horizontal heterogeneity around 0.7.

4. Discussion

The plantation and heavily logged treatments differed significantly from unlogged and lightly logged treatments in a number of parameters of vegetation structure and avian community composition. Despite a high rate of native plant colonization (Chapman and Chapman, 1996), the plantation’s avifauna was highly impover- Fig. 1. Observed and estimated bird species richness values. Based on ished. Thirty-one percent of the forest-dependent bird methods provided in EstimateS (Colwell, 1997). The solid bars are the species detected during the study were not observed at observed numbers of species and the ‘‘error bars’’ indicate the range of HL, in spite of its high overall bird species richness. In species richness estimates provided by EstimateS. addition, the study took place during dry season, when most bird species were not breeding and would be was calculated, values for forest sites ranged from 65 to expected to be less habitat-specific. UL and LL were 71%, but this proportion for PL was 38% (Fig. 2). almost identical in terms of vegetation structure and Yellow-whiskered greenbul (Andropadus latirostris) was about 85% of the forest-dependent bird species present/ the most abundant species in each treatment. The 10 predicted at UL were also present/predicted at LL, species with the highest number of observations made which indicates that at low intensities, selective extrac- up about 40% of the total counts in the forest treat- tion may have limited long-term impact on some forest ments, while this figure was 75% for PL. bird communities.

3.3. Effects of vegetation structure on bird species 4.1. Differences in vegetation structure richness LL did not exhibit significant differences from UL in Average canopy closure, tree diameter-at-breast- any aspects of vegetation structure measured in this height and index of horizontal heterogeneity for plots study, which agrees with previous research (Struhsaker, all showed significant correlations (P<0.01) with overall 1997). The low intensity of initial logging seems to have species richness and abundance of birds detected during prevented increased natural disturbance and made it surveys in plots. This was the case both when non-PL possible for the vegetation structure to revert to that of sites were examined separately and when PL was inclu- unlogged forest. ded. The correlations were negative for canopy closure On the other hand, three decades after logging, the and diameter-at-breast-height, and r2 values were vegetation structure of HL was still significantly differ- around 0.20. For these variables, the correlations ent from the vegetation structure of other treatments. were not significant when calculated for forest-depen- There was significantly less canopy closure, the average dent and non-forest birds separately (r2 <0.09, DBH was significantly lower and the trees were sig- P>0.05). The correlation was positive, however, for nificantly further apart. There were more than three index of horizontal heterogeneity (for non-PL plots times fewer trees >50 cm DBH in HL than at LL and only, r2>0.42 and P<0.0001; for all plots, r2>0.56 and at UL. 234 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240

Fig. 2. Rank abundance plots of bird species observed. The most common species, yellow-whiskered greenbul (Andropadus latirostris), was not included because its high abundance at all sites (Appendix) obscures the diﬀerences between species distribution curves. The log–series distribution of PL reﬂects its low species richness.

rate of natural treefall hinders the reestablishment of forest cover. PL was characterized by signiﬁcantly lower diversity of tree DBH distribution (likely indicating limited recruitment) and a more uniform spacing of trees, which make PL signiﬁcantly less heterogeneous in terms of vegetation structure than the non-plantation treatments.

4.2. Diﬀerences in bird communities

Even though the field work for this study was limited to 3 months, the bird community compositions of UL and HL were similar to those reported in Dranzoa’s (1998) multi-year study and are unlikely to be artifacts of the relatively short but intensive sampling period. High similarity values between the bird communities of LL and UL indicate that these treatments were more similar to each other than either was to HL. The lower Fig. 3. Intermediate values of horizontal heterogeneity of vegetation result in highest overall abundance and species diversity in plots. For- number of primary forest species detected at LL may be estNO and ForestSP refer to cumulative abundance and species partially explained by its location to a frequently used 3- diversity values at HL, LL and UL plots. PlantationNO and Planta- m wide dirt road (Karambi road), but the presence of a tionSP refer to corresponding values in PL plots. highly secretive and shy understory specialist like green- breasted pitta (Pitta reichenowi) at LL indicates good These results parallel the past findings of significantly potential habitat for sensitive primary forest understory lower canopy closure, foliage diversity index, basal area specialists. Only a few timber trees were extracted from of trees, and number of stems, and significantly higher parts of LL (C. Chapman, personal communication), rates of treefall, undergrowth, and densities of ele- which may have contributed to the persistence of most phants, deer, rodents, and other seed predators at HL forest-dependent bird species. when compared to UL and LL (Skorupa and Kasenene, HL exhibited higher overall bird species richness 1984; Isibirye-Basuta and Kasenene, 1987; Struhsaker et than UL, LL and PL. As was also recorded by Dran- al., 1996; Chapman and Chapman, 1997). Skorupa and zoa (1995, 1998), however, the high species richness of Kasenene (1984) also noted that in Kibale, beyond a HL was mainly a result of the presence of many non- threshold of logging disturbance of about 25%, the high forest species (Fig. 1). The infusion of non-forest C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 235 species, such as white-chinned prinia (Prinia leucopo- abundance, except those of non-forest birds, which gon) and blue-headed coucal (Centropus monachus), is would not be expected to be dependent on forest struc- thought to be caused by ‘‘vertical compression’’, tural diversity. The abundance and species richness of reduced canopy cover and increased open habitat all birds, as well as those of forest-dependent and forest making it possible for an abundance of non-forest and generalist species graphed separately, reached an forest edge species to be present in addition to forest asymptote at intermediate values of horizontal hetero- interior species (Thiollay, 1997; Dranzoa, 1995). Also, geneity of vegetation structure. Lowest overall abun- significantly fewer birds were recaptured with mist nets dance of forest birds was observed at PL, where trees at HL than were recaptured at UL (w2=4.92, P<0.05) were most homogeneously distributed. Compared to or LL (w2=6.61, P<0.05; C. Sekercioglu, unpublished UL and LL, the forest bird abundance values were also data), indicating that many forest birds may be tran- lower at HL, where the variation in tree distribution sients going through HL while moving between the was highest. unlogged areas around HL (Dranzoa, 1995). It is likely that forest birds were negatively affected by Out of the 59 forest-dependent species detected during the highly homogeneous tree distribution at PL as a the course of the study in all treatments, six were not result of the number of niches being limited since patchy observed at UL, whereas 18 were not found at HL, five habitats are considered to provide more diverse nesting of which were terrestrial understory specialist insecti- and foraging resources than locally uniform areas vores, (such as red-tailed ant-thrush, Neocossyphus (Roth, 1976). In addition, forest-dependent birds rufus), a group that was also shown to be sensitive to declined at highly heterogeneous HL where there were forest disturbance in other studies (Thiollay, 1997; many large, open patches avoided by forest-dependent Dranzoa, 1998; Aleixo, 1999; Sekercioglu et al., 2002). birds (Dranzoa, 1995). It is possible that the number of The species that were not observed at HL had low niches and/or the area of suitable habitat available for abundances at UL and LL, so it is possible that some forest birds is maximized at intermediate values of hor- were present at HL at densities below the detectability izontal heterogeneity where there is sufficient variation threshold. However, HL had the biggest sample size, in forest structure but not many large, open patches. had more open vegetation structure and hence better visibility, and all the richness estimators (Colwell, 1997) predicted about 20 fewer forest-dependent species at HL 5. Conclusion and recommendations than at UL and about eight fewer than at LL. These figures indicate that even after three decades, the high- Even three decades after selective logging took place level of initial disturbance at HL, exacerbated by in Kibale, its effect on forest structure and on the bird increased wind, shrub, rodent and elephant densities, community was still discernible, especially where the has prevented the reformation of complete forest cover, intensity of logging was highest. Of the vegetation resulting in the long-term loss of a large number of structural variables examined, horizontal heterogeneity forest-dependent bird species, even though mostly intact of vegetation had by far the most significant, positive forest surrounds HL (Struhsaker, 1997). relationship with abundance and richness of tropical Forty-eight forest-dependent species detected at other forest birds. In some temperate areas, increased hor- sites were not found at PL. Overall bird species richness izontal heterogeneity has been shown to correlate sig- was less than a third of that observed in other treat- nificantly with increased bird species richness (Roth, ments. Compared to the native forest treatments, fewer 1976; Berry and Bock, 1998) and increased nesting suc- species dominated the samples and there were fewer rare cess (Nolte and Fulbright, 1996). The results of this species. Although PL is also surrounded by mostly study suggest that more attention should be given to intact primary forest and has had high recruitment of horizontal heterogeneity in tropical habitats. indigenous tree species (Chapman and Chapman, 1996), Selective logging in the tropics is compatible with the the low richness and abundance of forest-dependent preservation of forest only when it is truly selective, not species indicate that most native bird species were only of the trees that are taken, but also, in terms of the unable to establish resident populations. A few bird total number of trees that are destroyed through logging species dominated the plantation at the expense of many and related activities. This study provides support for forest-dependent species that most likely disappeared the fact that selective timber extraction can be compa- as a result of the combination of low structural and tible with the preservation of the structural and biolo- botanical diversity. gical integrity of a tropical forest when logging intensity is kept below a certain threshold and parts of the log- 4.3. Vegetation structure and bird species richness ging compartment are left unlogged to provide source populations of forest organisms. Above that threshold, Horizontal heterogeneity showed a highly significant natural disturbance patterns are likely to delay the relationship with all measures of bird species richness or formation of the original forest cover significantly and 236 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 result in the disappearance of some forest-dependent especially indebted for his encouragement and support. species, as was the case in Kibale National Park. Permission to conduct this research was given by the Adherence to low-impact guidelines and ecologically Ugandan Forest Department and the directors of sound harvest cycles in tropical logging operations can Makerere University Biological Field Station, G. Isa- provide good habitat for many tropical forest species, as birye-Basuta and J. Kasenene. L. Bennun and R. well as being more economically profitable in the long- Wrangham provided invaluable help throughout the run (Putz et al., 2000). In addition to providing valuable project. G. Backhurst and J. Penhallurick provided me ecosystem services (Daily, 1997) such as water purifica- with indispensable bird bands and tapes of bird calls, tion and carbon sequestration, selectively logged forests respectively. C. A. Chapman and L. J. Chapman gave me can be significant additions to the limited network of considerable advice on Kibale throughout my research. strictly protected areas. K. Deo’s assistance was crucial for gathering data. I am grateful to P. Ashton, C. Boggs, M. C. Devine, M. Eve- lyn, J. Hellmann, J. Hughes, M. Leighton, T. Ricketts Acknowledgements and especially to my BA advisors R. Paynter and N. Pierce and PhD advisors G. Daily and P. R. Ehrlich for Funding for this research was provided by the Explor- their assistance in preparing this paper. I thank C. ers Club, Goelet Fund, Harvard University, Sigma Xi Chapman, M. W. Schwartz and D. Sheil for their con- Scientific Society and W. Loewenstern, Jr., to whom I am structive suggestions on improving this manuscript.

Appendix. Numbers of bird species observed during surveys at each compartment

ForDep is the degree of forest dependence based on Bennun et al. (1997). FD indicates forest-dependent, FG indicates forest generalist and NF indicates non-forest species. AFGIN, Aerial foraging insectivore; FRGR, Frugivore- Granivore; FRIN, Frugivore-Insectivore; FRUG, Frugivore; GRIN, Granivore-Insectivore; NECIN, Nectarivore- Insectivore; PRIN, Predator-Insectivore; SALIN, Sallying Insectivore; TUSIN, Terrestrial-understory insectivore; UFGIN, Understory foliage-gleaning insectivore; BGIN, Bark-gleaning insectivore. Nomenclature based on Clements (2000).

Guild ForDep Family and common name Scientiﬁc name UL LL HL PL Total Accipitridae RAPT FD Crowned Hawk-Eagle Sthephanoaetus coronatus 2010 3 Phasianidae GRIN FG Scaly Francolin Francolinus squamatus 1120 4 Numididae GRIN FG Crested Guineafowl Guttera pucherani 1045019 Columbidae FRGR FG African Green-pigeon Treron calva 766019 FRGR FG Tambourine Dove Turtur tympanistria 992020 FRGR NF Blue-spotted Wood Dove Turtur afer 0013 4 FRUG FD Rameron Pigeon Columbia arquatrix 2000 2 FRGR FD Afep Pigeon Columbia unicincta 434011 FRGR FD Lemon Dove Columba larvata 1200 3 FRGR NF Red-eyed Dove Streptopelia semitorquata 3391328 Psittacidae FRUG FD Gray Parrot Psittacus erithacus 2100 3 Musophagidae FRUG FG Great Blue Turaco Corythaeola cristata 12 11 12 0 35 FRUG FD Black-billed Turaco Tauraco schuettii 6310019 Cuculidae AFGIN FG Red-chested Cuckoo Cuculus solitarius 11 15 7 8 41 AFGIN FD Dusky Long-tailed Cuckoo Cercococcyx mechowi 13 11 7 0 31 AFGIN FD Olive Long-tailed Cuckoo Cercococcyx olivinus 0020 2 AFGIN FG African Emerald Cuckoo Chrysococcyx cupreus 1488030 AFGIN FG Yellowbill Ceuthmochares aereus 4230 9 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 237

Appendix (continued)

Guild ForDep Family and common name Scientific name UL LL HL PL Total PRIN NF White-browed Coucal Centropus superciliosus 0450 9 PRIN NF Blue-headed Coucal Centropus monachus 0111012 Strigidae RAPT FG African Wood-owl Strix woodfordii 0100 1 Trogonidae SALIN FG Narina Trogon Apaloderma narina 1099432 Alcedinidae SALIN FG Blue-breasted Kingfisher Halcyon malimbica 3400 7 SALIN NF African Pygmy-kingfisher Ispidina picta 2001 3 Coraciidae SALIN FD Blue-throated Roller Eurystomus gularis 2200 4 Phoeniculidae BGIN FD White-headed Woodhoopoe Phoeniculus bollei 611100 27 Bucerotidae FRUG NF Crowned Hornbill Tockus alboterminatus 5110 7 FRUG FG Black-and-white-casqued Ceratogymna subcylindricus 2175134 Hornbill Capitonidae FRUG FG Gray-throated Barbet Gymnobucco bonapartei 1100 2 FRIN FG Speckled Tinkerbird Pogoniulus scolopaceus 535013 FRIN FG Yellow-rumped Tinkerbird Pogoniulus bilineatus 10 9 12 7 38 FRUG FD Yellow-spotted Barbet Buccanodon duchaillui 466016 FRUG FG Hairy-breasted Barbet Tricholaema hirsuta 544013 FRIN FG Yellow-billed Barbet Trachyphonus purpuratus 1028020 Indicatoridae AFGIN NF Lesser Honeyguide Indicator minor 0010 1 AFGIN FD Willcock’s Honeyguide Indicator willcocksi 1100 2 Picidae BGIN FD Tullberg’s Woodpecker >Campethera tullbergi 0100 1 BGIN FG Brown-eared Woodpecker Campethera caroli 415616 BGIN NF Cardinal Woodpecker Dendropicos fuscescens 0010 1 BGIN FG Golden-crowned Woodpecker Dendropicos xantholophus 3020 5 Eurylaimidae SALIN FD African Broadbill Smithornis capensis 527216 Pittidae TUSIN FD African Pitta Pitta angolensis 1000 1 TUSIN FD Green-breasted Pitta Pitta reichenowi 0100 1 Pycnonotidae FRIN FD Plain Greenbul Andropadus curvirostris 526013 FRIN FG Little Greenbul Andropadus virens 12 10 18 8 48 FRIN FG Yellow-whiskered Greenbul Andropadus latirostris 79 82 107 66 334 FRIN FD Slender-billed Greenbul Andropadus gracilirostris 947020 FRIN FD Eastern Mountain-greenbul Andropadus nigriceps 2130 6 FRIN FD Toro Olive-greenbul Phyllastrephus hypochloris 0030 3 UFGIN FD White-throated Greenbul Phyllastrephus albigularis 9163028 FRIN FD Honeyguide Greenbul Baeopogon indicator 4400 8 FRUG FD Joyful Greenbul Chlorocichla laetissima 10 5 16 2 33 FRIN NF Common Bulbul Pycnonotus barbatus 0263543 UFGIN FD Common Bristlebill Bleda syndactyla 20 10 13 6 49 UFGIN FG Yellow-spotted Nicator Nicator chloris 1649433

(Appendix continued on next page) 238 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240

Appendix (continued)

Guild ForDep Family and common name Scientific name UL LL HL PL Total Timaliidae TUSIN FD African Hill Babbler Illadopsis abyssinica 2000 2 TUSIN FD Brown Illadopsis Illadopsis fulvescens 21 9 11 1 42 TUSIN FD Pale-breasted Illadopsis Illadopsis rufipennis 1000 1 TUSIN FD Scaly-breasted Illadopsis Illadopsis albipectus 956020 Turdidae TUSIN FD Brown-chested Alethe Alethe poliocephala 4311 9 TUSIN FD Red-tailed Ant-thrush Neocossyphus rufus 5300 8 TUSIN FD White-tailed Ant Thrush Neocossyphus poensis 4210 7 TUSIN FD Rufous Flycatcher-thrush Neocossyphus fraseri 2120 5 TERIN FG Olive Thrush Turdus olivaceus 0200 2 TERIN NF African Thrush Turdus pelios 341311 Muscicapidae SALIN FG Ashy Flycatcher Muscicapa caerulescens 0026 8 SALIN FG Dusky-blue Flycatcher Muscicapa comitata 2210 5 SALIN FD Gray-throated Tit-flycatcher Myioparus griseigularis 0100 1 TUSIN FD Equatorial Akalat Sheppardia aequatorialis 8133024 TUSIN FG Blue-shouldered Robin-chat Cossypha cyanocampter 6514025 TUSIN FG Red-capped Robin-chat Cossypha natalensis 721010 Sylviidae UFGIN FG Green Hylia Hylia prasina 4410018 UFGIN FD Black-faced Rufous-warbler Bathmocercus rufus 2210014 UFGIN NF Tawny-flanked Prinia Prinia subflava 0030 3 UFGIN FG Banded Prinia Prinia bairdii 0270 9 UFGIN FG White-chinned Prinia Prinia leucopogon 0213318 UFGIN NF Gray-backed Camaroptera Camaroptera brachyura 11 11 23 27 72 AFGIN FD Olive-green Camaroptera Camaroptera chloronata 848222 AFGIN FD Masked Apalis Apalis binotata 534719 AFGIN FD Buff-throated Apalis Apalis rufogularis 3230 8 AFGIN FD Black-throated Apalis Apalis jacksoni 2110 4 AFGIN FD White-browed Crombec Sylvietta leucophrys 1030 4 AFGIN FG Green Crombec Sylvietta virens 0010 1 Zosteropidae AFGIN NF African Yellow White-eye Zosterops senegalensis 8 5 12 18 43 Paridae AFGIN FD Dusky Tit Melaniparus funereus 12 10 5 0 27 Monarchidae SALIN NF African Blue-Flycatcher Elminia longicauda 0100 1 SALIN NF African Paradise-Flycatcher Tersiphone viridis 0001 1 SALIN FD Black-headed Paradise-Flycatcher Tersiphone rufiventer 4481430 Platysteiridae SALIN FD African Shrike-Flycatcher Megabyas flammulatus 1110 3 SALIN NF Black-and-white Shrike-Flycatcher Bias musicus 4221 9 SALIN NF Brown-throated Wattle-eye Platysteira cyanea 3330 9 SALIN FD Chesnut Wattle-eye Platysteira castanea 1230 6 SALIN FD Jameson’s Wattle-eye Platysteira jamesoni 2030 5 Malaconotidae UFGIN FG Gray-green Bushshrike Telophorus bocagei 0050 5 UFGIN FG Luehder’s Bushshrike Laniarius luehderi 219012 UFGIN NF Tropical Boubou Laniarius aethiopicus 0040 4 AFGIN FD Pink-footed Puffback Dryoscopus angolensis 1120 4 UFGIN FG Brown-crowned Tchagra Tchagra australis 2021216 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240 239

Appendix (continued)

Guild ForDep Family and common name Scientific name UL LL HL PL Total Campephagidae FRIN FD Petit’s Cuckoo-shrike Campephaga petiti 341210 Dicruridae SALIN FG Fork-tailed Drongo Dicrurus adsimilis 4210 7 Oriolidae FRIN FD Black-tailed Oriole Oriolus percivali 3100 4 FRIN FG Western Black-headed Oriole Oriolus brachyrhyncus 14 11 18 22 65 Sturnidae FRUG FD Narrow-tailed Starling Poeoptera lugubris 2200 4 FRUG FD Chesnut-winged Starling Onychognathus fulgidus 1110 3 FRUG FG Purple-headed Glossy-Starling Lamprotornis purpureiceps 4131 9 Nectariniidae NECIN FG Collared Sunbird Hedydipna collaris 1160 8 NECIN FD Western Olive-Sunbird Cyanomitra obscura 13 9 17 20 59 NECIN FD Blue-headed Sunbird Cyanomitra alinae 4220 8 NECIN FG Green-headed Sunbird Cyanomitra verticalis 0200 2 NECIN FG Green-throated Sunbird Chalcomitra rubescens 0020 2 NECIN NF Variable Sunbird Cinnyris venustus 049013 NECIN FG Olive-bellied Sunbird Cinnyris chloropygius 0010 1 NECIN FG Scarlet-chested Sunbird Chalcomitra senegalensis 0030 3 Ploceidae GRIN NF Grossbeak Weaver Amblyospiza albifrons 0010 1 GRIN NF Black-necked Weaver Ploceus nigricollis 0020 2 GRIN NF Spectacled Weaver Ploceus ocularis 0020 2 GRIN FD Black-billed Weaver Ploceus melanogaster 1010 2 GRIN NF Vieillot’s Weaver Ploceus nigerrimus 0020 2 GRIN FD Yellow-mantled Weaver Ploceus tricolor 1000 1 GRIN FG Forest Weaver Ploceus bicolor 15 9 18 27 69 BGIN FD Red-headed Malimbe Malimbus rubricollis 3050 8 Estrildidae UFGIN FD Woodhouse’s Antpecker Parmoptila woodhousei 1020 3 AFGIN FG Gray-headed Negrofinch Nigrita canicapilla 2010 3 AFGIN FG White-breasted Negrofinch Nigrita fusconata 0021 3 FRIN NF White-collared Oliveback Nesocharis ansorgei 0010 1 GRIN FG Red-faced Crimson-wing Cryptospiza reichenovii 0002 2 GRAN FG Red-headed Bluebill Spermophaga ruficapilla 2043 9 GRAN FD Green-backed Twinspot Mandingoa nitidula 0020 2 Total 589 452 657 340 2038

References Berry, M.E., Bock, C.E., 1998. Eﬀects of habitat and landscape char- acteristics on avian breeding distributions in Colorado foothills Abramovitz, J.N., Matoon, A.T., 1999. Reorienting the forest pro- shrub. The Southwestern Naturalist 43, 453–461. ducts economy. In: Starke, L. (Ed.), State of the World 1999: A Bibby, C.J., Burgess, N.D., Hill, D.A., Mustoe, S., 2000. Bird Census Worldwatch Institute Report on Progress Toward a Sustainable Techniques. Academic Press, London. Society. W.W. Norton & Company, New York. Chapman, C.A., Chapman, L.J., 1996. Exotic tree plantations and the Aleixo, A., 1999. Eﬀects of selective logging on a bird community in regeneration of natural forests in Kibale National Park, Uganda. the Brazilian Atlantic forest. The Condor 101, 537–548. Biological Conservation 76, 253–257. Anonymous, 2001. What is Selective Logging? (WWW document). Chapman, C.A., Chapman, L.J., 1997. Forest regeneration in logged Accessed 6 April 2001. Available at: http://www.biology.duke.edu/ and unlogged forests of Kibale National Park, Uganda. Biotropica bio217/esh5/page2.html. 29, 396–412. Bennun, L., Pomeroy, D., Dranzoa, C., 1997. The forest birds of Chazdon, R.L., Colwell, R.K., Denslow, J.S., Guariguata, M.R., Kenya and Uganda. Journal of East African Natural History 85, 1998. Statistical methods for estimating species richness of woody 23–48. regeneration in primary and secondary rain forests of NE Costa 240 C.H. Sekercioglu / Biological Conservation 107 (2002) 229–240

Rica. In: Dallmeier, F., Comiskey, J.A. (Eds.), Forest Biodiversity Magurran, A.E., 1988. Ecological Diversity and Its Measurement. Research, Monitoring and Modeling: Conceptual Background and Princeton University Press, Princeton, NJ. Old World Case Studies. Parthenon Publishing, Paris, pp. 285–309. Nolte, K.R., Fulbright, T.E., 1996. Nesting ecology of scissor-tailed Clements, J.F., 2000. Birds of the World: A Checklist. Ibis Publishing, flycatchers in south Texas. Wilson Bulletin 108, 302–316. Vista, CA. Nummelin, M., 1990. Relative habitat use of duikers, bushpigs and Colwell, R.K., 1997. EstimateS: Statistical Estimation of Species Rich- elephants in virgin and selectively logged areas of Kibale Forest, ness and Shared Species from Samples. Version 6 (WWW document). Uganda. Tropical Zoology 3, 111–120. Accessed 5 June 2001. Available at: www.viceroy.eeb.uconn.edu/ Oksanen, L., 2001. Logic of experiments in ecology: is pseudoreplica- estimates. tion a pseudoissue? Oikos 94, 27–38. Colwell, R.K., Coddington, J.A., 1994. Estimating terrestrial biodi- Pinard, M.A., Putz, F.E., 1996. Conserving forest biomass by reducing versity through extrapolation. Philosophical Transactions of the logging damage. Biotropica 28, 278–295. Royal Society (Series B) 345, 101–118. Putz, F.E., Dykstra, D.P., Heinrich, R., 2000. Why poor log- Daily, G. (Ed.), 1997. Nature’s Services: Societal Dependence on ging practices persist in the tropics. Conservation Biology 14, 951– Natural Ecosystems. Island Press, Washington, DC. 956. Dranzoa, C., 1995. Bird Populations of Primary and Logged Forests Putz, F.E., Blate, G.M., Redford, K.H., Fimbel, R., Robinson, J., in Kibale Forest National Park, Uganda. PhD dissertation, 2001. Tropical forest management and conservation of biodiversity: Makarere University, Uganda. an overview. Conservation Biology 15, 7–20. Dranzoa, C., 1998. The avifauna 23 years after logging in Kibale Repetto, R., Gillis, M. (Eds.), 1988. Public Policies and the Misuse of National Park, Uganda. Biodiversity and Conservation 7, 777–797. Forest Resources. Cambridge University Press, Cambridge. Isibirye-Basuta, G., Kasenene, J.M., 1987. Small rodent populations Roth, R.R., 1976. Spatial heterogeneity and bird species diversity. in selectively felled and mature tracts of Kibale Forest, Uganda. Ecology 57, 773–782. Biotropica 19, 260–266. Sekercioglu, C.H., Ehrlich, P.R., Daily, G.C., Aygen, D., Goehring, Jennings, S.B., Brown, N.D., Sheil, D., 1999. Assessing forest canopies D., Sandı´, R.F., 2002. The disappearance of insectivorous birds and understory illumination: canopy closure, canopy cover and from tropical forest fragments. Proceedings of the National Acad- other measures. Forestry 72, 59–73. emy of Sciences 99(1), 263–267. Johns, A.D., 1985. Selective logging and wildlife conservation in tro- Skorupa, J.P., Kasenene, J.M., 1984. Tropical forest management: can pical rain forest: problems and recommendations. Biological Con- rates of natural treefalls help guide us? Oryx 18, 96–101. servation 31, 355–375. Struhsaker, T.T., Lwanga, J.S., Kasenene, J.M., 1996. Elephants, Johns, A.D., 1988. Effects of ‘‘selective’’ timber extraction on rain selective logging and forest regeneration in the Kibale Forest, forest structure and composition and some consequences for frugi- Uganda. Journal of Tropical Ecology 12, 45–64. vores and folivores. Biotropica 20, 31–37. Struhsaker, T.T., 1997. Ecology of an African Rain Forest: Logging in Johns, A.D., 1992. Vertebrate responses to selective logging: implica- Kibale and the Conflict Between Conservation and Exploitation. tions for the design of logging systems. Philosophical Transactions University Press of Florida, Gainesville, FL. of the Royal Society of London 335, 437–442. Thiollay, J., 1997. Disturbance, selective logging and bird diversity: a MacArthur, R.H., MacArthur, J.W., 1961. On bird species diversity. neotropical forest study. Biodiversity and Conservation 6, 1155– Ecology 42, 594–598. 1173.