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Abundance and Distribution of Sympatric Gibbons in a Threatened Sumatran Rain Forest
Timothy G. O’Brien,1,3,4Margaret F. Kinnaird,1,3Anton Nurcahyo,2 Mohamed Iqbal,2and Mohamed Rusmanto2
Received March 11, 2003; revision June 23, 2003; accepted July 21, 2003
Agile gibbons (Hylobates agilis) and siamangs (Symphalangus syndactylus) are sympatric small apes inhabiting threatened forests of Sumatra, Indonesia.
We censused both species in the 3,568-km2 Bukit Barisan Selatan National Park, at the southern limit of their ranges, over a 7-mo period in 2001. First, we monitored daily calling rates from known populations to develop probabilities of calling during a specified number of days and used the probability of calling at≥1 time during 3 days to convert calling rates to abundance. Next, we used 3-day calibrated call count censuses (n=31) stratified by distance from forest edge and across a range of elevations to estimate species-specific group densities. We used group size from the known populations as well as data collectedad libitumduring the census to convert group density to individual density. Agile gibbon group density averaged 0.67 km−2 (SE =0.082) and group size averaged 2.6 (SE=0.73) for a population estimate of 4,479 (SE= 1,331) individuals. Siamang group density averaged 2.23 km−2(SE=0.245), and group size averaged 3.9 (SE=1.09) for a population estimate of 22,390 (SE=8,138). Agile gibbon and siamang densities are negatively correlated, with agile gibbons more abundant in mid-elevation forests and siamangs most abundant in lowland and submontane forests. The small group sizes of agile gibbons indicate potential survival problems in infant and juvenile size classes.
Although neither species is presently threatened by direct human disturbance,
1Wildlife Conservation Society - Asia Program, 2300 Southern Blvd, Bronx, New York 10460.
2Wildlife Conservation Society - Indonesia Program, P.O. Box 311, Bogor 16003, Indonesia.
3Present address: National Center for Ecological Analysis and Synthesis, 735 State St., Suite 300, Santa Barbara, California 93101.
4To whom correspondence should be addressed; e-mail: [email protected].
267
0164-0291/04/0400-0267/0°C2004 Plenum Publishing Corporation
continued deforestation will jeopardize the long-term viability of both species in Bukit Barsian Selatan National Park and on Sumatra.
KEY WORDS: Agile gibbon; siamang; census; Sumatra; Indonesia.
INTRODUCTION
Rain forest primate populations are threatened pantropically as a re- sult of deforestation, trade in wild meat and, to a lesser extent, the pet trade (Robinson and Bennett, 2000; Robinson and Redford, 1991). The problem is especially acute in Asia, which has more critically endangered primate species than any other tropical region (IUCN, 1996). Efforts to address pri- mate conservation issues in Asia are hampered by a lack of knowledge about population sizes and demographic characteristics of most species. Unhab- ituated forest primates are difficult to census and to study (Brockelman and Srikosamatara, 1993; Nijman, 2002). Consequently, there are relatively few estimates of population size or density for Asian primates, especially over landscapes greater than a few km2. Thus, policy makers and managers usually rely on approximations and educated guesses to develop conser- vation strategies, management plans and estimates of population viability (Harcourt, 2002). Asian gibbons (Hylobatidae) are especially vulnerable and poorly understood. Although gibbons have been the subjects of many behavioral and ecological studies since the 1930s (Bartlett, 1999; Carpenter, 1940; Chivers, 1974; Leighton, 1986; Preuschroftet al., 1984), few data are available to examine population and demographic trends in this important primate family (Mitani, 1990; O’Brienet al., 2003a).
Gibbons occur throughout Southeast Asia in primate communities of
≥12 species (Brandon-Jones et al., 2004; Gupta and Chivers, 1999; Reed, 1999). Reed (1999) finds that Asian primate communities have the highest proportion of primate species and biomass distributed in the 5–10 kg-body size range that includes the gibbons. Gibbons make upca.7–20% of primate density andca.10–25% of the primate biomass in these communities. In any given community however, there are only 1–2 gibbon species (Hylobates, Symphalangus), co-occurring with similarly-sized leaf monkeys, macaques, and, on Sumatra and Borneo, the larger orangutan.
Agile gibbons (Hylobates agilis) and siamangs (Symphalangus syndacty- lus) occur sympatrically in peninsular Malaysia and on Sumatra, Indonesia.
Both species are highly territorial, mostly monogamous and use morning loud songs for territorial advertisement and defense (Chivers, 1974;
Cowlishaw, 1992). Siamangs are considerably larger than agile gibbons (11 and 6 kg, respectively; Schultz, 1973) and are more folivorous than gibbons in Peninsular Malaysia (Chivers, 1974, 1984). However, both species are
primarily frugivorous on Sumatra (Nurcahyo, 1999; O’Brien, unpublished data; Palombit, 1997). Agile gibbons and siamangs are protected through- out their range (local laws, CITES Appendix I, IUCN Low Risk, not threat- ened): on Sumatra, they are threatened by forest conversion and oppor- tunistic collection for the pet trade. These threats extend to populations in national parks and protection forests (Jepsonet al., 2001; Kinnaird et al., 2003; O’Brienet al., 2003a).
We used calibrated point count surveys and censuses of group compo- sition (Brockelman and Srikosamatara, 1993; Nijman, 2002) to determine the distribution, density, and population sizes of agile gibbons and siamangs at the southern limit of their range in the Bukit Barisan Selatan National Park of southern Sumatra. We also assessed the effects of human proximity on siamang and agile gibbon densities by examining differences in density near the forest boundary versus in the forest interior. Finally we examined how altitude and forest type affects the distribution and co-occurrence of siamangs and agile gibbons (Chivers, 1974; Yanuar, 2001).
METHODS Study Area
Bukit Barisan Selatan National Park (BBSNP) is the third largest pro- tected area (3,568 km2) on Sumatra (Figure 1) of which 2,568 km2remains under forest cover (Kinnairdet al., 2003). The remaining land is deforested scrubland, illegal gardens and coffee plantations (O’Brien and Kinnaird, 2003). Located in the extreme southwest of the island (4◦310– 5◦570S and 103◦340– 104◦430E), the park spans the provinces of Lampung and Bengkulu for more than 150 km along the Barisan Mountain Range. Elevation ranges from sea level in the south to 1800 m asl in the north. BBSNP contains some of the largest tracts of lowland rain forest remaining on Sumatra and is the major watershed for southwest Sumatra. The park is bordered by villages, agriculture and plantation forestry. The park’s thin elongate shape results in
>700 km of borders, and encroachment for logging and agriculture are ma- jor problems. Two roads bisect the park in the north and the south creating three large forest blocks. Rainfall is weakly seasonal and normally ranges from 3000 mm to more than>4000 mm except during El Ni ´no – Southern Oscillation (ENSO) events when droughts occur. Temperatures normally fluctuate from 22◦to 35◦C but daytime maximum temperatures may exceed 40◦C.
The Way Canguk Research Station is in the southern part of BBSNP (5◦3903200S, 104◦2402100E; Fig. 1) at 50 m elevation, in a mosaic of primary
Fig. 1.Location of Bukit Barisan Selatan National Park on Sumatra and Sunda Sunda shelf (inset), and distribution of sampling locations in the park.
forest, and forest damaged by fire, drought, wind throws, and earthquakes.
The study area encompasses 900 ha of forest, is split by the Canguk River, and is crossed by trails at 200-m intervals. The area is contiguous to large tracts of undisturbed lowland forest, but has active illegal logging within 3 km and agricultural activity within 5 km.
Calibration: Distance Between Calling Groups
Gibbons are difficult to census because they tend to occur high, in thick canopy, rarely come to the ground, are very wary, and have unpredictable re- sponses to detection of humans ranging from noisy flight to quiet hiding. For these reasons, Brockelman and Ali (1987) and Nijman (2002) recommend the use of point counts (Bibbyet al., 1992; Bucklandet al., 1993) to circum- vent problems associated with limited visibility of gibbons in the canopy and the variable response of gibbons to detection by humans.
Use of call counts to estimate population size of gibbons may result in double counting groups. To avoid counting groups twice, Brockelman
and Srikosamatara (1993) recommended that groups calling>500 m apart be considered distinct. For siamangs, we assessed the relationship between calling and position to determine the likelihood that two calls might belong to the same group. We analyzed movements for 3 habituated siamang groups from 120 all-day follows between April – July 2000 and April – July 2001.
Between 0630 h and 1200 h, we recorded group location and calculated the straightline distance moved from the original position to subsequent positions in 30-min intervals. We also calculated the straightline distance moved between calling bouts on days when groups called more than once to determine the range of distances moved between calls. We restricted the analysis to April-July, the same period during which we conducted the park- wide survey.
To determine the range of maximum distances that agile gibbons might move between calls, we approximated gibbon home ranges as circles corre- sponding to published home range sizes for several species (Leighton, 1986;
Mitani, 1990; Palombit, 1992) and used the diameter of the circles as the maximum distance between calls of a single group. While this may underes- timate the maximum distance across an irregularly shaped home range we included hypothetical ranges of≤70 ha, an area much larger than published gibbon home ranges.
Calibration: Probability of Calling
We estimated the probability of calling within a given time period by conducting call count surveys in the Way Canguk research area using a known population of siamang and gibbon groups. Between January and March 2002, we counted calls on 36 mornings in 3 intervals of 5, 10 and 21 days duration. Between 0500 h and 1200 h, 3 observers listened for call- ing siamang and agile gibbon groups. When a group called, we used a digital compass to determine angle of call, independently estimated distances to calling groups, and then compared results. We recorded weather conditions at 10-min intervals, including cloud conditions (subjectively rated as clear,
<50% cloud cover,>50% cloud cover), rain versus no rain, and wind, sub- jectively rated as calm, breezy and windy. We also recorded the minimum temperature the night preceding the sample.
We mapped results each day and determined the number of groups of each species calling from call location. We arbitrarily eliminated groups calling>2 km from the station because we believe that we cannot reliably hear groups further away. We also eliminated solo calling male agile gib- bons from consideration since it is not possible to determine if a solo-calling male is a dispersing individual or a resident of a group (Brockelman and
Srikosamatara, 1993). We overlaid calling positions on maps of known and approximate group ranges developed during 5 yr of census work in the area (O’Brien, unpublished data) and assigned calls to the closest group. We cal- culated probabilities of calling on a single day and calling once in a 2-day, 3-day, 4-day and 5-day interval for each species. Although calling rates may vary between years, there is no consistent pattern among months (Kinnaird, unpubl. data) and we assume our calling rates are representative for any given month.
Park Census
We conducted calling counts of siamangs and agile gibbons in BBSNP between April and July 2002. We divided sampling sites evenly between forest edge and forest interior. We defined sampling points≤2 km of the forest boundary as forest edge and ones≥2 km from the forest boundary as forest interior. We chose samples randomly in 10-km north-south intervals to ensure a representative coverage of the park and the range of elevations.
Forest interior samples were subject to the constraint that travel time to the sample point be≤2 days from the edge of the park. As a result, edge and interior points were usually≤10 km of one another. We sampled each point for 3 days. We collected data via three teams working simultaneously but at different locations. Each team comprised an observer who participated in the calibration study and an assistant.
We calculated group density based on the area of a circle of 2-km radius (12.57 km2). We reduced an area proportionately if observers could not hear beyond high ridges or part of the sample area was deforested (Brockelman and Ali, 1987; Brockelman and Srikosamatara, 1993). We assessed forest cover and topography based on a recent analysis of forest cover (Kinnaird et al., 2003), a digital elevation map, and a delineation of watershed bound- aries (WCS-IP, unpublished data) using ARCVIEW 3.2 GIS software.
We calculated group density for agile gibbon and siamang at each census location (i) as:
DGi=mi·p−1·(1i·5·r2)−1 (1) where in DGi=group density (km−2) in the ith location, mi=number of distinct groups heard over a 3-day period, p=probability of a group calling during a 3-day period,1i=proportion of circle from where a group could be heard, and r=the radius from which groups could be heard (2.0 km in this study). Variance in group density for a given location (S2Gi) is simply:
S2Gi=D2Gi·s2p·p−2 (2)
where in s2p=the variance in probability of calling (Brockelman and Ali, 1987). Because we have unequal sampling areas across locations, the av- erage group density for the park (DG) is weighted by the area sampled:
DG=(6iAi·DGi)·(6iAi)−1 (3) where in Ai=1i·5·r2 and defines the area of each sample i. The vari- ance in estimates of group densities associated with areas of varying size is:
S2G=D2G·¡
6iA2i ·s2m/p¢
·A−2·((6iAi·mi·p−1)·A−1)−1 (4) where in s2m/p=the variance of the estimated number of groups across lo- cations (Krebs, 1989). To estimate the number of siamang and agile gibbon groups in the park (GPark), we expanded the density from (3) to the en- tire forested area of the park and used the variance for sampling without replacement per Jolly (1969):
S2G-Park=N·(N−n)·n−1·(n−1)−1·
(6i(mi·p−1)2+D2G-Park·6iA2i −2·DG-Park·6imi·p−1·Ai) (5) where in N=number of 2-km radii sample points and is estimated by the area of forest divided by 12.56 km2(204 potential samples), n = number of samples.
Finally, we calculated population estimate for the park (PPark) as the parkwide group estimate multiplied by average group size (I):
PPark=GPark·I (6)
with an associated variance of:
S2P=P2Park·¡
S2G-Park·G−2Park+S2I·I−2¢
(7) where in S2Iis the variance in group size (Bucklandet al., 1993). We collected group size data for siamang and agile groups during annual censuses in Way Canguk research area between 1998 and 2002 and opportunistically during the park survey (O’Brienet al., 2003a; unpublished data).
RESULTS
Calibration: Movement and Distance Between Calling Groups Siamangs.Siamang groups make their greatest movements from the point of origin (usually the sleeping tree) within the first 3 h of daily activity
Fig. 2.Percentage of straightline distances from point of origin to sia- mang locations in 30-min intervals over a 3-h period beginning at 0630 h.
and the movements rarely exceed 500 m. They tend to move in small half- hour increments of<100 m (83% of half-hour movements: Figure 2). As the time interval increased up to 3 h, the average distance from origin increased as well but>90% of movement over all time intervals considered is≤350 m.
After 3 h, distance from origin tends to decline and by 6 h, most groups had backtracked toward the point of origin ( ¯X2000±SD=253±210; ( ¯X2001± SD=255±149). Focal siamang groups called>1 time per day on 22 days. The distance moved between calls ranged from 0 to 378 m (( ¯X=96±99 m). We concluded that a 500-m cut-off to distinguish between calling groups is justi- fied and conservative for siamangs (Brockelman and Srikosamatara, 1993).
Agile Gibbons.Gibbons have home ranges of 7–58 ha (Bartlett, 1999;
Leighton, 1986; Mitani, 1990). Assuming that average home ranges are cir- cular, the range diameters vary from 50 m to 370 m. An exceptionally large home range of 70 ha has a diameter of 472 m. We therefore applied a con- servative 500 m separation for calling groups to incorporate the ellipsoid nature of many home ranges.
Calibration: Probability of Calling
Siamangs.We recorded 316 calling siamang groups during 36 days of sampling at Way Canguk. Groups called on 591 occasions, indicating that on some days groups called more than once. By mapping the location of calls on
known siamang home ranges within the study area and mapping locations of consistent calling outside the study area, we estimate the total number of groups within a 2-km hearing radius at 45 groups or 3.6 groups/km−2. There were 37 groups of siamangs whose territories occurred at least partially within the study area in 2001 (O’Brienet al., 2003a), including 2 recently established groups that failed to call during the sample period. The density of calling groups in the study area is thus somewhat<3.9·km−2depending on how much of the edge home ranges occur within the study area.
Among the siamang groups that were systematically followed, 97% of calls during a 12-h period occurred before 1200 h. During the calibration trials, 80% of all siamang calling occurred before 1000 h. On average, 24%
of the groups within 2 km called on a given day. Weather did not have a strong influence on daily calling rates by siamangs. Calling was unaffected by minimum temperature the night before, maximum daytime temperatures, rainfall in the 24 period before a sample, or cloudy skies. Calling is nega- tively correlated with breezy weather conditions (r= −0.38, P=0.023) and proportion of time that it rained during the sample (r= −0.31, P=0.066), but neither effect is especially strong. Rainy and breezy conditions are not correlated. Rainfall occurred more often during the hours leading up to the 0700–1000-h peak in calling, whereas breezy conditions increased immedi- ately after the peak in calling.
The probability of calling on a given day for siamangs is 0.246 (±0.120:
Fig. 3) but rose quickly to 0.535 (±0.192) for the probability of calling≥1 time during a 3-day period. After 3 days, incremental increases in calling rate are low and by day 5 the likelihood of calling≥1 time is 0.682 (±0.191), a 15%
increase. The variance appears to stabilize by day 3 and, though spending more time listening increases the likelihood that all groups will be heard, the additional 2 days of sampling do not result in a reduction in variance.
Agile Gibbon.We recorded 151 agile gibbon calling bouts represent- ing 12 agile gibbon groups ≤2 km of the census point, for a density of 1 group/km−2. Among the 9 groups that used the study area, all groups called
≥1 time during the calibration trials for a calling density ofca.1 group/km−2. Agile gibbons called most frequently between 0600 and 0800 h (65% of calling) and rarely called after 1000 h (4% of calling). As with siamangs, weather did not have a strong effect on the daily likelihood of calling by agile gibbons. Agile gibbons tended to call less on mornings with a high pro- portion of rain during sampling (r= −0.377, P=0.023) and called more on cloudless days (r=0.357, P=0.033). However, neither effect is particularly strong. Wind, temperature and rainfall before sampling had no detectable effect on variation in daily calling.
The probability of calling on a given day for agile gibbons is 0.417 (±0.241: Fig 3) but rose quickly to 0.750 (±0.198) for the probability of
Fig. 3.Probability of calling (with standard deviation)≥1 time during a 1-day to 5-day interval for agile gibbons (open bars) and siamang (hatched bars).
calling≥1 time per 3-day period. After 3 days, incremental increases in call- ing rates are low and by day 5 the likelihood of calling ≥1 time is 0.891 (±0.131), a 14% increase. Unlike siamangs, variance appears to stabilize by day 4, indicating that additional time devoted to sampling may improve the precision of the estimate.
Given the tradeoffs between increased likelihood of hearing all groups and reduced variance associated with longer per point sampling effort, the time constraint of collecting an adequate number of samples and not violat- ing closed population assumptions (Bucklandet al., 1993), and the time and financial constraints of working in an inaccessible park, we chose to conduct the park survey via 3-day samples. We then corrected the number of groups detected by the probability of calling once during a 3-day period to estimate the number of groups/sample.
Abundance and Distribution
Siamang groups are 3 times more abundant than agile gibbons groups throughout the park (Table I: Paired T=5.035, df=30, P<0.0001) and group densities for siamangs and agile gibbons are negatively correlated (r= −0.523, P=0.003). Neither siamangs nor agile gibbons appear to avoid forest edges (2-sample Tsiamang = 1.04, df=29, P=0.305; Tgibbon =0.2, df=29, P=0.843), suggesting that proximity to humans is not an important factor in the distribution of either species.
Both species were affected by elevation (Figure 4). Gibbon group den- sity displayed a significant convex quadratic response to elevation (Dgibbon
Table I.Siamang and gibbon population estimates for Bukit Barisan Selatan National Park, Sumatra, based on current forest cover estimates
Parameter Agile gibbon Siamang
Range of group density (DGi) 0–1.76 km−2 0.4–4.82 km−2 Park density (DG; SE) 0.67 km−2(0.082) 2.23 km−2(0.245)
# groups in park (GPark; SE) 1,716 (173) 5,741 (441)
95% CI 1,377–2,055 4,876–6,606
Average group size WC (I) 2.61 (0.73) 3.9 (1.09) Average group size park 2.71 (0.76) 3.75 (0.96) Population size in park (PPark) 4,479 (1,331) 22,390 (8,138)
CV 29.7% 36.3%
Note.Parameter symbols are in parentheses.
=0.05+0.003·Elevation – 2.3·10−6·Elevation2, F2,28=22.2, P<0.001).
Gibbon groups occurred in only 3 of 9 samples below 150 m, whereas densi- ties peaked ( Dgibbon=1.1 groups km−2) at mid-elevations. Siamang group densities showed a significant concave quadratic response (Dsiamang=3.85+
Fig. 4.Distribution of siamang and agile gibbon group densities by elevation and location relative to forest edge. Regression lines show quadratic relationships be- tween group density (agile gibbon - solid line; siamang - dashed line) and elevation.
0.007·Elevation+4.5·10−6·Elevation2, F2,28=9.957, P=0.001). Siamang group densities peak below 300 m (Dsiamang =3.3 grps km−2), while mid- elevation densities were lowest (Dsiamang=1.2 grps km−2). Densities above 1000 m are intermediate for both species, but higher for siamangs than for agile gibbons. Overall, elevation accounts for 42% of variation in siamang densities and 61% of variation in agile gibbon densities across the park.
As in the calibration trials, weather appeared to have little effect on the daily number of calls per group (calculated by number of detected groups). Weather conditions were overwhelmingly clear (68.3 % of sampling time) and calm (64.4% of sampling time). Agile gibbon and siamang calling are weakly correlated with breezy conditions (rgibbon= −0.225, P=0.033, rsiamang= −0.239, P=0.024), but overall, breezy conditions accounted for
<6% of the variation in daily calling by siamangs and gibbons. Rainy sample periods are correlated with cloudy periods (r=0.273, P=0.009) and nega- tively correlated with windy conditions (r= −0.271, P=0.010). Cloudy skies are negatively correlated with breezy conditions (r= −0.313, P=0.003).
We estimated the number of groups in the park by expanding the weighted average park density to all forest in the park. The current esti- mate of forest cover for BBSNP is 2,568 km2(Kinnairdet al., 2003), which may support≤1,716 agile gibbon groups and 5,741 siamang groups (Table I).
Average group size varied among siamangs and gibbons in Way Canguk and in the park survey, but the differences are not significant. Agile gibbon group size averaged 2.61 in Way Canguk and 2.71 individuals in the park survey.
Siamang groups averaged 3.9 individuals in Way Canguk and 3.75 in the park sample. We used the Way Canguk figure to estimate the park popu- lation because we are more certain of group compositions in Way Canguk, where groups have been censused since 1998. Final park population esti- mates are 4,479 agile gibbons and 22,390 siamangs (Table I). The estimates have large error terms associated with them, and CV is almost 30% for agile gibbons and 36% for siamangs due to the large inherent variability in the group sizes rather than poor precision of the estimates. Siamang estimates may be slightly higher if we include newly formed groups in an area that may not call. In Way Canguk, 5% of all siamang groups did not call but the groups represent only 3% of the population.
DISCUSSION
Our results indicate that healthy populations of agile gibbons and sia- mangs persist at the southern limit of their ranges in Bukit Barisan Selatan National Park. Although BBSNP is fragmented into 3 large forest blocks and deforestation and human disturbance are persistent problems (Kinnaird
et al., 2003; O’Brienet al., 2003b), agile gibbon and siamang populations number in the thousands. Populations of this size should persist over the long-term (Harcourt, 2002) if the park maintains its present forest area and illegal hunting and habitat degradation are stopped.
We estimate 5 times as many siamangs in BBSNP as agile gibbons. The lowest group densities of siamangs are comparable to the highest group densities of agile gibbons. The smaller average group size of gibbons means that point densities of agile gibbons are lower than siamangs at all eleva- tions. Range-wide, densities and average group size of agile gibbons tend to increase from southern to northern latitude on Sumatra, Borneo and Peninsular Malaysia (Table 2). Contrarily, siamang densities tend to decline from south to north while variability in group size shows no trend. BBSNP lies at the southern extreme of the density gradients, where agile gibbons are at their lowest densities range-wide and siamangs are near their highest densities.
Table II. Density estimates for agile gibbon and siamang (ind./km2) by forest type for our study (calculated using Laumonier 1990 definitions of altitudinal forest zones) and from other
studies on Sumatra, Borneo and Malaysia
Location Agile gibbon Siamang Habitat Reference
BBSNP 1.4 10.3 Lowland forest This study
2.8 4.2 Hill forest
2.2 6.7 Submontane
forest
Way Kambas, Sumatra 1.9 2.8 Lowland forest Yanuar and Sugardjito, 1993
0 0 Swamp forest
Kerinci Seblat, Sumatra 6.0 24.6 Lowland forest Yanuar, 2001
11.4 7.2 Hill forest
10.8 11.4 Submontane
forest
0 18.4 Montane forest
Ketambe, Sumatra Not present 5.0 Lowland forest West, 1981 7.0 Lowland forest MacKinnon and
MacKinnon, 1980 Sumatra, island wide 8.6 9.0 Lowland forest Wilson and Wilson,
1977 Gunung Palung, Borneo 13.5–15.6 Not present Lowland, Hill, Mitani, 1990
Swamp forest
Sungai Dal, Malaysia 18.92 2.4 Gittins and
Raemaeker, 1980 Ulu Sempan, Malaysia Not present 6.0 Hill forest Chivers, 1974 Kuala Lompot, Not present 5.0 Lowland forest Chivers, 1974
Malaysia
Ulu Gombak Not present 2.4 Hill forest Chivers, 1974
North Malaysia 6.12 No data Lowland, hill Chivers, 1974 forest
Density gradients may be related to diet, forest structure and compo- sition, and demography. Siamangs are more folivorous in Malaysia than on Sumatra (Chivers and Raemakers, 1986; Nurcahyo, 1999; Palombit, 1997).
Palombit (1997) attributes the increased frugivory by siamangs (and lar gib- bon) in Leuser National Park, northern Sumatra, to increased feeding on large patches of strangling figs rather than increased feeding on other fruits.
In BBSNP, siamangs also consume large amounts of figs from canopy-size strangling figs, but they also exploit canopy-sized patches ofDracontomelum dao(Anacardiaceae; Nurcahyo, 1999; O’Brienet al., 2003a), a species that apparently does not occur in Ketambe, Leuser National Park (de Wilde and Duyfjes, 1996; Palombit, 1992) or in Peninsular Malaysian study sites (Chivers, 1974). Higher availability of figs and other canopy-sized fruit trees on Sumatra may increase dietary overlap between agile gibbons and sia- mangs, as Palombit (1997) reported for lar gibbons and siamangs in north- ern Sumatra. Accordingly, the siamang’s larger body size and longer feeding bouts may give them a competitive advantage over agile gibbons in exploit- ing the large food patches.
Agile gibbons appear to do very well in forests dominated by trees of the Dipterocarpaceae: agile gibbon densities peak in the hill dipterocarp forests of Kerinci Seblat National Park, (17.9% Dipterocapraceae; Yanuar, 2001), located only 100 km north of BBSNP. The highest agile gibbon densities from Peninsulan Malaysia (Gittins and Raemaeker, 1980) and Borneo (Mitani, 1990) also occur in dipterocarp-dominated forests. In BBSNP, hill forests rich in dipterocarps constitute<25% of the forest cover (Kinnairdet al., 2003;
M. Iqbal, personal observation). Tree density also appears to increase from south to north. Tree density (trees≥10 cm DBH) is 434 trees/ha−1in BBSNP lowland forest, 501 trees/ha−1(>10 cm diameter) in Kerinci Seblat National Park (Yanuar, 2001) and≤800 trees/ha−1in Peninsular Malaysia (Bennett, 1983; Caldecott, 1982; Marsh and Wilson, 1981). Gupta and Chivers (1999) showed that primate community biomass increases as tree density increases due to increased availability of food trees and cover. This relationship is not significant for sites within Peninsular Malaysia, and Marsh and Wilson (1981) speculated that dipterocarp forests there had lower primate densities (and community biomass) than other forest types because the dominance of dipterocarps resulted in fewer fruits. However, lower community density does not mean that all species occur at lower density. Given the agile gibbon’s small body size relative to that of siamangs, and small group size relative to those of other frugivorous primates, they may be better suited to feed in the smaller fruit patches that characterize dipterocarp forests than larger primates or larger groups of similar sized primates.
Differences in forest structure and composition may explain the differ- ences we observed in agile gibbon and siamang densities at mid-elevations:
agile gibbons attained high densities and siamangs reached their lowest den- sities. Yanuar (2001) reported the same trend of high agile gibbon and low siamang densities in mid-elevation dipterocarp forests in Kerinci Seblat National Park. The mid-elevation forests of BBSNP are characterized by higher densities of dipterocarp trees (M. Iqbal, personal observation). Sia- mangs occur in highest densities in lowland forests, the dominant forest type in BBSNP (Kinnairdet al., 2003). Thus, what appears to be an elevation ef- fect may in fact reflect a preference for dipterocarp forests by agile gibbons and an avoidance of them by siamangs.
Agile gibbon average group size (2.61 individuals: Table I) is smaller in BBSNP versus other parts of their range, which contributes to a lower density of individuals. In Kerinci Seblat NP, the agile gibbon population has an average group size of 3.0 (Yanuar, 2001), whereas on Borneo (Mitani, 1990) and in Peninsular Malaysia (Gittins and Raemaeker, 1980) average group size is 4.1 and 4.4, respectively. Conversely, siamang group size in BBSNP, is within the normal range for gibbons (Leighton, 1986). The small group size of agile gibbons in BBSNP may result from reduced survival in the early age classes, longer interbirth intervals, or both. In BBSNP, min- imum interbirth interval for agile gibbons is 3.3 yr (O’Brien, unpublished data), which is similar to the value reported for Borneo (3.2 years: Mitani, 1990). Therefore, the most likely explanation for small group size is that early survival rates for agile gibbons are lower versus those on Borneo.
O’Brienet al. (2003a) found that siamang group size in BBSNP is signifi- cantly affected by lower infant and juvenile survival in small groups versus large groups. Since agile gibbons are at the southern limit of their range in BBSNP, where dipterocarp forests are uncommon, and survival rates may be low, the park’s forests may be sufficient but suboptimal habitat for the species. Siamangs appear to benefit from the abundance of lowland habitat, strangling figs and Dracontomelum dao, and lack of dipterocarp forest.
Agile gibbon and siamang groups apparently are more tolerant of hu- man disturbance than other mammals are in BBSNP, most likely due to a lack of harassment by humans. For example, pigtailed macaques (Macaca nemistrina), are twice as common in areas with low human population on the park boundary and mouse deer (Tragulusspp.) are almost 10 times more common (O’Brienet al., 2003b). Pigtailed macaques are agricultural pests and mouse deer are hunted for food. Gibbons and siamangs are not eaten by local people, nor are they agricultural pests. Although gibbons and siamangs are often found in the illegal pet trade, there are no data to suggest that they are hunted specifically for trade. We suspect that pet trade in agile gibbons and siamangs is a by-product of logging; they are collected when the forest is cut down and then sold to traders.
Long-term persistence of agile gibbons and siamangs in BBSNP will require the Indonesian government to regain control over illegal deforesta- tion of the park. Kinnairdet al. (2003) reported that between 1985 and 1999 lowland forest cover in the park declined from 54% to 40% and hill - sub- montane - montane forest declined from 26% to 12% cover. Meanwhile agriculture development inside the park has doubled, mostly for production ofCaffea robusta. O’Brien and Kinnaird (2003) showed that deforestation rates in BBSNP are tightly linked torobusta coffee prices. Since BBSNP coffee plantations have no canopy, they provide no habitat for siamangs or gibbons. On a larger scale, forests are threatened throughout Sumatra (Holmes, 2001; Jepsonet al., 2001): between 1995 and 2000, almost 40% of gibbon and siamang habitat on Sumatra was damaged or destroyed by fire, logging and conversion to agriculture or plantations (O’Brien, unpublished data). While siamang and agile gibbon populations appear secure today, their futures are uncertain and will depend on vastly improved conservation efforts, especially in Sumatra’s remaining parks and protected areas.
ACKNOWLEDGMENTS
Our research is a collaborative effort by the Wildlife Conservation Soci- ety – Indonesia Program and the Indonesian Ministry of Forestry’s Depart- ment for Protection and Conservation of Nature (PHKA). The research was funded by the Wildlife Conservation Society, the U.S. Fish and Wildlife Ser- vice Great Apes Conservation Fund (Grant #98210-1-G084) and the Disney Conservation Fund. We thank Pedet, Aris, Teguh, Wariono, and Bawuk for assistance with data collection, our colleagues in PHKA for their support, and D. Chivers for helpful insights on an earlier draft.
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