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Artificial nest and seed predation experiments in tropical lowland rainforest remnants of Singapore
BIOLOGICAL CONSERVATION
ELSEVIER
Biological Conservation 85 (1998) 97-104
Artificial nest and seed predation experiments in tropical lowland rainforest remnants of Singapore Timothy C.M. Wong, Navjot S. Sodhi *, I.M. Turner t School of Biological Sciences, National University of Singapore, Kent Ridge, Singapore 119260, Republic of Singapore Received 16 March 1997; accepted 27 August 1997
Abstract
Tropical lowland rainforests of Southeast Asia are continually being fragmented and lost at an alarming rate. Little is known about the consequences of this large-scale habitat modification. Using artificial nest and seed experiments, we determined predation rates in forest remnants (2.5-1100 ha in area) of Singapore and Pulau Ubin. Singapore (641 km2) is highly urbanised with only 5% of the native forest cover remaining, whereas Pulau Ubin (11 km2) is relatively less developed with about 60% of the native forest cover remaining. We specifically determined if predation rates varied in relation to: (i) distance from edge, (ii) forest types, (iii) forest areas, (iv) isolation, (v) edge to area ratio, (vi) canopy closure, and/or (vii) area (Singapore vs Pulau Ubin). Overall, 80.5% (n = 328) of artificial ground nests were depredated, of which 55.3% were predated by small mammals. For seeds, 98.2% (n = 219) experimental stations were predated. Generally, the predation rate did not vary significantly in relation to the distance from the edge, though a primary forest remnant had lower artificial nest and seed predation rates than the other remnants. Pulau Ubin remnants were found to have lower predation rates than remnants on Singapore island. No significant correlations were found between predation rates and remnant area, isolation from other remnants, or the edge/area ratio, or canopy density. Relatively high predation rates in some tropical secondary and primary forest remnants may greatly influence plant regeneration and bird community structure. © 1998 Elsevier Science Ltd. All rights reserved Keywords." Fragmentation; Negative edge effects; Nest predation; Seed predation
I. Introduction
Due to human activities (e.g. agriculture and settlements), large forest tracts are continually being fragmented into smaller patches. Forest fragmentation and loss can have deleterious consequences for the native biota (Whitcomb et al., 1981). Because it results in greater edge (Hoover et al., 1995), generalized predators that are adapted to edge habitats can more easily penetrate forest remnants than similar continuous forests (Whitcomb et al., 1981; Wilcove, 1985). Documentation of high predation rates in forest remnants is thus important from a conservation perspective as such a phenomenon can have dire consequences for avian reproductive success and seedling establishment (Burkey, 1993). Because actual predation events are hard to observe, one indirect way to determine how well bird and plant species may be reproducing in fragments is through * Corresponding author. Fax: + 65-874-2486; e-mail: [email protected] t Present address: Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA. 0006-3207/98/$19.00 © 1998 Elsevier Science Ltd. All rights reserved PII: S0006-3207(97)00145-6
artificial nest and seed predation experiments. The nest and possibly seed predation in forest patches may depend on a number of factors including patch size, distance from edge, and/or habitat age and structure (Gates and Gysel, 1978; Chasko and Gates, 1982; Wilcove, 1985; Yahner and Wright, 1985; Andr~n and Angelstam, 1988; Picman, 1988). From a conservation perspective, it also is important to identify the factors that may influence predation rates in forest remnants. Despite alarming rates of forest loss and fragmentation in the tropics (Myers, 1988; Turner and Corlett, 1996), few studies have examined nest predation in fragmented tropical landscapes (e.g. Gibbs, 1991; Sieving, 1992; Loiselle and Hoppes, 1983). To our knowledge, no nest predation experiment has been conducted in the tropical lowland rainforests of Southeast Asia. It is therefore unknown if studies done in other regions can be applicable to this region. Apart from Burkey, 1993, no work on seed predation in relation to forest fragmentation within the tropics has been published. We experimentally tested whether the predation rate of nests and seeds are affected by (i) distance from edge,
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(ii) forest types, (iii) size of fragment, (iv) isolation, (v) edge to area ratio, and/or (vi) canopy closure. Also, we compared the predation rates between the main island of Singapore and those at another island, Pulau Ubin. We hope that with our study, the knowledge gained may influence decisions regarding forest harvesting practices within tropical rainforests of Southeast Asia.
2. Methods and materials 2.1. Study sites
We used eight forest fragments on two islands. Five study sites were on Singapore (area=641 kmZ), while the other three sites were on Pulau Ubin (11 kmZ). The native forested area of Singapore (103°50'E, l°20'N) and Pulau Ubin (103°57'E, 1°25'N) is about 5 and 60%, respectively (Turner et al., 1994). Singapore is one of the most densely populated areas, whereas Pulau Ubin is relatively little developed. The five study sites in Singapore included two primary forests (MacRitchie, Bukit Timah 1), two secondary forests (Bukit Timah 2, Central Catchment), and one abandoned rubber plantation (Teck Chong). The fragment, Bukit Timah Nature Reserve (Bukit Timah 2) is actually the secondary forest surrounding another study site, Bukit Timah 1, which is a primary forest. Of the three sites on Pulau Ubin, one was a secondary forest (Ubin 3) whereas the other two sites were abandoned rubber plantations (Ubin 1 and Ubin 2). The study fragments were surrounded by a variety of edges such as track, road, reservoir, and pipeline. The primary forest is defined as a remnant where the original forest cover is still present (Corlett, 1995), and where there are many large primary forest trees present, such as dipterocarps. Secondary forest is defined as the regrowth from disturbed primary forest where the break in continuity is still detectable in the structure and/or floristic composition of the vegetation (Corlett, 1994). The rubber plantation sites in this study were actually secondary forests (according to the above definition). But they were treated as rubber plantation sites because most of the trees found in these plots were rubber trees (Hevea brasiliensis). Forest remnants are defined as forested areas surrounded by unforested habitat on all sides. In this study, forest remnants, patches, sites, and fragments are used interchangeably. 2.2. Materials
For the nest predation experiment, chicken eggs were used. The use of chicken eggs served to simulate the eggs of the Red Jungle Fowl (Gallus gallus), a groundnesting bird which occurs in Pulau Ubin (pers. obs.). As suggested by both Janzen, 1978 and Whelan et al., 1994,
fresh chicken eggs (bought on the same day of experiment set-up) were used. Raw shelled peanuts were used for the seed predation studies. The use of peanuts served as the introduction of an 'exotic seed', thus giving estimates of predation rates that are from generalists, rather than specialist predators (Burkey, 1993). In addition to real eggs and seeds, plasticine eggs and peanuts, were also used. Plasticine was used to determine the type of predators that attacked the eggs and seeds by the bite-marks left on the plasticine (cf. Moiler, 1989; Langen et al., 1991). The imitation eggs and peanuts were hand-made from brown plasticine. The plasticine chicken eggs were then painted with poster colours to give a 'chicken-egg' colour. During the handling of the real and plasticine eggs and peanuts, rubber gloves were worn at all times to the reduce contamination with human scent. However, because of their smell, it is possible that painted plasticine eggs may have influenced the behaviour of certain types of predators. 2.3. Methods
Within each transect, there usually were five experimental stations. The number of transects at site A, B l, B2, C, D, E, F, G and H were 15, 5, 10, 15, 20, 16, 15, 15, and 10, respectively (Table 1). Each transect started from the edge of the forest (here defined as the first tree or shrub) and ran 100m into the forest, and each transect was arranged perpendicular to the edge. The five stations were demarcated at 0 (the edge), 25, 50, 75, and 100m. The egg experimental stations were located at the 0, 50, and 100m positions whereas the seed experimental stations were placed at the 25 and 75 m marks. At an egg experimental station, we placed one real chicken egg and one plasticine egg. At each seed experimental station, we placed five raw peanuts and five plasticine peanuts. All peanuts were placed in a petri-dish. Minimal markings were placed along the transect to avoid giving cues to potential predators. The experimental stations (eggs or peanuts) were placed at random distances (1-5m) and at random directions (left or right) of an experimental station. To facilitate relocation, they were usually placed near buttresses of trees or the base of larger saplings, as done by many previous researchers (e.g. Yahner et al., 1989; Gibbs, 1991; Rudnicky and Hunter, 1993; Vander Haegen and Degraaf, 1996; Yahner and Mahan, 1996). We attempted to cover the eggs and seeds by adjusting the vegetation, such that when viewed directly from above, at a height of 1.8 m, the percentage cover directly above the seeds and eggs was about 50%. The eggs were placed on the open ground and no attempt was made to create any artificial nests. Although no attempt was made to construct an artificial nest, we designate the egg experiment stations as nests because many ground nesting bird
T.C.M. Wong et al./Biological Conservation 85 (1998) 97-104
Table 1 Results of artificial nests predation rates, small mammal predation rates, and seed predation rates for all remnants. Figures in parentheses are number of experimental stations preyed over the total number of experimental stations Site
A B1 B2 C D E F G Total
H
Predation rates Nest
Small mammals
Seed
86.05% (37/43) 93.33% (14/15) 76.67% (23/30) 64.44% (29/45) 80.00% (48/60) 68.89% (31/45) 91.11% (41/45) 91.11% (41/45)
72.97% (27/37) 42.86% (6/14) 78.26% (18/23) 48.28% (14/29) 70.83% (34/48) 2%03% (9/31) 26.83% (11/41) 65.85% (27/41)
100.00% (30/30) 100,00% (10/10) 100.00% (20/20) 93.33% (28/30) 100.00% (40/40) 96.77% (30/31) 100.00% (28/28) 96.67% (29/30)
80-49% (264/328)
55.30% (146/264)
98.17% (215/219)
73.33% (44/60)
29.55% (13/44)
100.00% (60/60)
Site A: Teck Chong rubber plantation (area=35ha, edge/area ratio = 2-38, isolation = 250 m, canopy density= 88.2%). Site Bh Pulau Ubin rubber plantation I (Ubin 1) (2.5ha, 2.32, 240m, 83.3%). Site B2: Pulau Ubin rubber plantation 2 (Ubin 2) (170 ha, 1.30, 300 m, 88.6%). Site C: Pulau Ubin secondary forest (Ubin 3) (100ha, 2.26, 300m, 80.3%). Site D: Central Catchment (secondary forest) (ll00ha, 2.72, 420m, 90.2%). Site E: MacRitchie Reservoir Park (primary forest) (65ha, 2.10, 300 m, 94.9%). Site F: Bukit Timah Nature Reserve (primary forest) (Bukit Timah 1) (164 ha, 1-65, 620 m, 80.9%). Site G: Bukit Timah Nature Reserve (secondary forest) (Bukit Timah 2) (164 ha, 1.65, 620 m, 85-6%). Site H: Central Catchment (secondary forest); same as the site D but transect lengths in this experiment were extended up to 250 m into the forest.
species do not build elaborate nests. To minimize the possibility of attracting the attention of potential predators, we minimized the time spent at each station. The transects within a fragment were spaced 5 0 m away from each other (cf. Gibbs, 1991). Paths were not cleared along the transects and every effort was made to minimize the impact of setting up the experiment. The experiments were performed in August 1996, which is during the end of the birds' breeding season in Singapore (Hails and Jarvis, 1987). To avoid pseudoreplica-
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tion (Hurlbert, 1984), we conducted experiments only once at each site except one site (site D) where during a subsequent experiment, we extended the transects up to 250 m (see below). To determine the predation rates, experimental nest and peanut stations were checked on day 8, except for the site Ubin 2, which was checked on day 10. Nests were considered as preyed upon if: (i) an egg was missing, (ii) there were cracks or peck marks on the real chicken egg, (iii) the chicken egg was smashed, or (iv) bite-marks were on the plasticine eggs. Similarly, for the peanuts, the station was considered preyed upon if: (i) any of the peanuts were missing, or (ii) there were bitemarks observed on the plasticine peanuts. During the setting up and checking days, all sightings of potential predators (e.g, Corvus spp.) were recorded. Predation by small m a m m a l s was determined by examining the bite marks imprinted on the plasticine eggs and comparing these to teeth sizes of potential predators. The teeth sizes of potential predators were obtained from material in the Zoological Reference Collection, National University of Singapore. If a plasticine egg had incisor marks <2 m m wide, we considered it being predated by a small mammal. Incisor marks > 2 m m wide on plasticine eggs were considered to be predation by larger-sized mammals, Predation by avian predators was determined by the presence of beak marks on plasticine eggs. Similarly, other specific markings on plasticine eggs revealed predation by other predators such as reptiles. Because 100 m within the forest may still be considered as an edge (Kroosdma, 1984), we further performed an experiment in a fragment (Central Catchment) where the transect lengths were extended up to 250 m into the forest. The experimental stations were located at 0, 50, 100, 150, 200, and 250m. At each distance, both eggs and seeds were placed. The direction (left or right) in which the eggs or seeds were placed was determined randomly. The distance between neighbouring transects was 50 m. 2.4. M e a s u r e m e n t s o f variables
As suggested by Small and Hunter (1988), aerial photographs and topographical maps were used to determine the area and the edge length of each site. The fragment areas were determined by using an area measuring machine (Area Measurement System, DeltaT Devices Limited, UK). Edge/area index (SI) was obtained by measuring the perimeter of the fragment on the topographical m a p with a curvimeter, and substituting the values into the equation formulated by Patton (1975),
Edge/area index = circumference - x/(2 x zr × area)
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Isolation index was obtained by measuring the distance of the nearest forest plots (>4 ha in area) in the northern, eastern, southern, and western directions. These were averaged to give the isolation index (li) (Blake and Karr, 1987). Canopy density was also measured by using a spherical densiometer (Model A). At each distance demarcation of the transects, canopy density readings were taken in the four cardinal directions, and the canopy density for the experimental station was obtained by calculating the mean of these four readings (Lemmon, 1957).
2.5. Statistical analyses Non-parametric analysis of variance (Kruskal-Wallis ANOVA) was used to test whether transects within each site were significantly different from each other in terms of predation rates (Siegel and Castellan, 1988). The effect of distance from the edge on the predation rate was tested using the Kruskal-Wallis ANOVA for the eggs, and Mann-Whitney U test for the peanuts. G-statistic tests were used to determined if there were significant differences in predation rates among fragments with different sizes, and habitat types. Spearman-Rank Correlations were used to determine if there were any significant correlations between predation rates and canopy density, area of the fragment, isolation, or edge/ area ratio. Spearman-Rank Correlations were also used to detect for correlations between nest and seed predation rates. All statistical tests were conducted using STATVIEW. Significance level for all statistical tests was set at 0.05. Throughout the text, i refers to standard error.
detected for any of the fragments. Thus, this allowed the data from each fragment to be pooled for further analyses. No significant differences (ANOVAs, p > 0.16) were detected in nest predation rates relative to the distance from the edge for any of the fragments. The nest predation rate differed significantly among fragments (G = 20.667, d.f. = 7, p = 0.01; Table 1). There was also a significant difference in the nest predation rate among Singapore fragments (p = 0.02, Tables 1 and 2). A significant difference in nest predation rates was detected between the two primary forest fragments (/9=0.01, Table 2). Further analysis showed that MacRitchie (site E) had the lowest nest predation rate (P= 0.01) among the fragments on Singapore (Table 1). There was no significant difference in the nest predation rate among forest types for Pulau Ubin (p = 0.08, Table 2). Thus, these were pooled and compared with the Singapore fragments. There was a significantly higher (p=0-01) predation rate in Singapore (sites A + D + G ; mean predation rate=85.7+3.3%) than Pulau Ubin fragments ( B I + B 2 + C ; 78.1+8.5%) (Table 2).
3.2. Nest predation by small mammals Predation by small mammals was analysed to determine the intensity of small mammalian predation on eggs. No significant differences in small mammal predation rates were detected among transects within each fragment (ANOVAs, p > 0-26). Significantly different small mammal predation rates were detected among fragments (G=40.819, d.f.--7, p=0.01; Table 1). Small mammal predation rates also differed in relation to the Table 2 G-tests for difference in nest predation rates among forest types
3. Results
Site
Predation of artificial nests and seeds was observed at all sites (Table 1). Overall, 80-5% of the artificial nests were preyed upon, out of which 55.3% were preyed upon by small mammalian predators, and the rest by medium-sized mammals, birds, and monitor lizards (Varanus salvator). For seeds, 98.2% of the stations were preyed upon, with five fragments registering 100% predation rates (Table 1). Potential nest and/or seed predators observed at various sites include monitor lizard, crows, squirrels (Sundasciurus tenuis and Callosciurus notatus), wild pig (Sus scrofa), feral dog (Canis spp.), banded leaf monkey (Presbytis femoralis), and long-tailed macaque (Macaca fascicularis).
Singapore fragments All Primary Secondary Secondary (p) vs rubber Secondary (p) + rubber vs primary (Site E) Secondary (p) + rubber vs primary (Site F)
3.1. Nest depredation No significant differences (Kruskal-Wallis ANOVAs, p>0-10) in nest predation rates among transects were
Pulau Ubin fragments All Singapore and Pulau Ubin fragments Mainland-secondary (p) + rubber vs Ubin-secondary + rubber (p) Primary (Site E) against all other sites
G
d.f.
p
11.31 6.94 2.46 0.04 6.00 1.06
4 1 1 1 1 1
0.02* 0.01" 0.12 0.84 0.01" 0.30
5-06 2 0,08 7.36
1 0.01"
10.38 1 0.01"
Primary, Primary forests (Site E and Site F). Secondary, Secondary forests (Site C, Site D and Site G). Rubber, Rubber plantations (Site A, Site BI and Site B2). For site abbreviations, see Table 1. (p), Pooled data. * Significance at ~ = 0.05.
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distance from the edge for only two fragments (Table 3). Both sites A (of mammalian predation on 27 nests, 12, 8, and 7 nests were predated at 0, 50, and 100m, respectively) and B2 (of mammalian predation at 18 nests, 8, 6, and 4 were predated at 0, 50, and 100m, respectively) had the highest nest predation rates by mammals at 0 m and the lowest nest predation rates by mammals at 100m, with intermediate nest predation rates at 50 m. Small mammal nest predation rates differed significantly among forest types in Singapore fragments (p=0.01, Tables 1 and 4). Primary forests had significantly lower small mammal predation rates than all other forest types in Singapore (p=0.01, Tables 1 and 4). Significant differences in small mammal predation rates were also found for forest types in Pulau Ubin (p=0-03, Table 4). The rubber plantations exhibited significant differences in small mammal predation between the two fragments in Pulau Ubin (p=0.02). The fragment B2 had significantly higher small mammal predation rate than the other two sites on Pulau Ubin (Table 1). When Singapore sites (those that had no significant difference in small mammal predation rates, A+D+G; mean predation r a t e = 7 1 - 9 + l . 5 % ) were compared with Pulau Ubin sites (B1 + C ; 42.9+ 1.1%), higher predation was detected for Singapore sites (p=O.O1). 3.3. S e e d predation
No significant differences were detected among transects in seed predation rates within all fragments (ANOVAs, p > 0.45). Also, distance from the edge did not affect seed predation (Mann-Whitney U-tests, p > 0.15). The seed predation did not differ significantly among fragments ( G - 7 - 0 1 9 , d.f.=7, p=0.43; Table 1). Because of no significant variations in seed predation rates among fragments, further analyses were not carried out, bearing in mind that all the sites had similar predation rates (Table 1). Table 3 Kruskal-Wallis ANOVAs (KW) for difference in small mammal predation rates in relation to the distance from the edge Site
KW
d.f.
p
A B1 B2 C D E F G
5-91 1.63 5.94 O.44 0-48 3-55 0.50 4.03
2 2 2 2 2 2 2 2
0.05* 0.44 0.05* O-80 0.79 0.17 0.78 0-13
For site abbreviations, see Table 1. * Significanceat a = 0.05.
Table 4 G-tests for differencein small mammal nest predation rates among forest types Site
Singapore fragments All Primary Secondary Secondary (p) vs rubber Secondary (p) + rubber vs primary (p) Pulau Ubin fragments All Rubber Rubber (BI) vs secondary Rubber (B2) vs secondary Mainland-secondary (p)+rubber vs Ubin- secondary+ rubber (B1)
G
d.f.
p
33.16 0.04 0.25 0.25 33.70
4 1 1 I 1
0.01" 0-84 0.61 0.62 0-01"
7.20 5.85 0.19 5.66
2 1 1 1
0.03° 0.02" 0.66 0.02*
7.36 1 0.01"
* Significanceat a = 0.05.
N o significant correlation was found in nest and seed predation rates (rs=0.47, d.f.=8, p=0.22; Table 1). Also, no significant correlation between small mammal predation rates and seed predation was found (rs = 0.22, d.f. = 8, p = 0.56; Table 1). For extended transects, there were no significant differences among transects for nest predation rates ( K W = 15.42, d.f. = 9, p = 0.08), small mammal nest predation rates ( K W = 9.82, d.f. = 2, p = 0.37) and seed predation rates (KW=0.00, d.f. = 9, p = 1.00). Predation rate (nest, small mammal, or seed) differences in relation to the distance from the edge were also not detected (ANOVAs, p > 0-46). 3.4. Patch characteristics and predation rates
No significant correlations were found between predation rates (nest predation, small mammal predation, and seed predation) and the four variables (fragment area, edge/area ratio, isolation index, and canopy density) (all Spearman rank correlations, n =8, p > 0 . 3 3 ) (Table 1).
4. D i s c u s s i o n
Our results show that the predation rate on artificial nests and seeds is relatively high in tropical rainforest remnants of Singapore and Pulau Ubin than reported from similar studies elsewhere (e.g. Yahner and Wright, 1985; Andr6n and Angelstam, 1988; Gibbs, 1991; Burkey, 1993). The unusually high predation rates in Singapore and Pulau Ubin could be due to several reasons. First, matrix (area surrounding remnants) is highly urbanised, at least, in Singapore. Urban areas can harbour relatively high densities of potential
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predators such as feral animals (e.g. dogs) and corvids. Second, Singapore is one of the highly fragmented landscapes with only 5% of the native forest cover remaining. This may have resulted in many potential predators (e.g. monkeys) being confined only to remaining pockets of forests. Last, it is possible that our experiment design (using of artificial painted eggs) may have resulted in high levels of predation of artificial nests. Singapore remnants usually revealed higher nest predation rates than those at Pulau Ubin. Nest predation rates on islands are usually higher than those at comparable mainland sites (Loiselle and Hoppes, 1983; Nilsson et al., 1985), which is attributed to the high density of small to medium-sized predators on islands. However, our study shows that predation rates may differ among different islands. The lower predation rates in Pulau Ubin could be due to several factors such as higher native forest cover than Singapore and it is still less developed, both of which may have resulted in lesser influx of generalist feral predators (e.g. feral dogs) and human associated predators (e.g. corvids) there. Or it may be due to the notion that smaller islands have lower species diversity (including predators) and abundance than larger islands (MacArthur and Wilson, 1967). We found the variation in nest predation rates among some of our remnants. However, the patch variables that we measured (remnant area, isolation, edge/area ratio, and canopy density) failed to reveal significant correlations with predation rates. Different studies have attributed correlations of artificial nest predation rates with different variables such as canopy density, area, isolation, vegetation, and edge/area ratio (e,g. Burkey, 1993; Major and Kendal, 1996). The lack of a correlation between predation rates and various patch variables in our study can be due to the variables that we did not measure (e.g. density and abundance of potential predators), which may more strongly affect the predation rates. We found most cases of nest predation by mammals (all sizes combined; 71.9%), with only 6.1% nest predation attributed to avian predators. This is different from a number of previous studies which reported high avian predation of artificial nests (Andrrn et al., 1985; Angelstam, 1986). One reason for the high mammalian nest predation in Singapore could be due to the habitat surrounding the edge. In several similar studies in temperate regions, the edge consisted of pasture lands or farmlands (Yahner and Wright, 1985; Yahner and Cypher, 1987). Corvids are usually abundant in such edges as they either scavenge for food in the farmlands, or they may search for nests in the pasture or forested areas. In Singapore, isolated forests are usually surrounded by urbanised areas. Corvids can be abundant in urban areas, but in Singapore, they are considered as pests and are controlled by the Primary Production
Department of Singapore by regular shooting. Artificial predation rates have been found to be higher at edges than forest interior in several studies (Gates and Gysel, 1978; Brittingham and Temple, 1983; Wilcove, 1985; Burkey, 1993). Distance effects (higher predation rates at forest edge vs forest interior) were usually attributed to the increase in potential nest predators along the edge (Andrrn and Angelstam, 1988). Such potential nest predators include corvids as well as mammals (Yahner and Scott, 1988; Yahner and Voytko, 1989). In contrast, however, there are also a number of studies the results of which do not support higher predation rates at edges than forest interior (Angelstam, 1986; Ratti and Reese, 1988; Small and Hunter, 1988; Nour et al., 1993; Hanski et al., 1996). It has also been suggested that at edges, there is higher predation by avian predators than in forest interiors. However, this may be compensated for by a rise in mammalian predation because in a heavily fragmented landscape, such as Singapore, forest-dwelling mammals may be confined to forest fragments. Thus, the net effect was that predation rates remained relatively constant, and thus, no distance effect was detected in most cases, even for the experiments with transect lengths of 250 m. No significant correlation was found between nest and seed predation rates, even though there was a high correlation coefficient for nest and seed predation rates (rs--0.47). This could probably be due to the small sample size. It would therefore seems to be reasonable to expect a high predation rate for nests if there was a high predation rate for seeds, since both nests and seeds were exposed to similar types of predators. Also, no significant correlation was found between small mammal nest predation and seed predation rates, which again may be an artefact of small sample size. 4.1. Implications and limitations Southeast Asia is considered to be a one of the megabiodiversity regions (Briggs, 1996). However, deforestation in this region is predicted to cause mass species extinctions (Wilson, 1992; Brooks et al., 1997). Despite this, rainforests in Southeast Asia are continually being cleared and fragmented at an alarming rate (Turner and Corlett, 1996) and there appears to be no clear guidelines for reserve area and cut-block designs. Artificial and natural predation rates may differ (Willebrand and Marcstr6m, 1988). Because our study is only based on artificial predation rates, it is not known to what extend our study is indicative of natural predation rates. Experiments, such as ours, likely determine predation pressure by generalist predators and thus are suitable for community-level nest/seed vulnerability (Sieving, 1992) and at best only provide an estimation of relative predation rates (Loiselle and Hoppes, 1983; Wilcove, 1985).
T.C.M. Wong et al./Biological Conservation 85 (1998) 97-104
Our study also is done in one of the highly urbanised landscapes (Singapore), therefore, it is not known how applicable our study will to other forested landscapes in the region. However keeping the above limitations in mind, some postulations/recommendations can be derived from our study. First, many forest flora and fauna have already gone extinct within Singapore (Turner and Corlett, 1996). It is possible that relatively high level of predation rates because of high level of fragmentation may be one of the factors influencing the extinctions of certain forest flora and fauna from Singapore. Second, considering that high predation rates were observed in remnants as large as l l00ha and in those that were relatively less disturbed (primary forests, Table 1), there is an urgent need for studies similar to ours from various landscapes and forest types of Southeast Asia. Data from these studies can then be used by local conservation and government agencies to critically examine forest harvesting practices within Southeast Asia. In this study, we have been dealing with ground nests. Experiments should be carried out on studies with domed and pouch nests, which provide more protection and concealment from predators than open-cup nests (Ricklefs, 1969), and are more common among tropical, forest breeding birds (Ricklefs, 1969; Gibbs, 1991). Nests of tropical birds may also be more dispersed temporally than nests in temperate forests because the breeding seasons of tropical, wet forest birds are longer, extending over much of the year (Gibbs, 1991). Thus, temporal artificial nest predation studies may reveal certain yet unknown trends.
Acknowledgements The authors thank Dr. Hugh Tan, Mr. Tommy Tan, Benjamin Lee, and Janet Nichol for help. They are grateful to the National Parks Board of Singapore for permission to carry out research in nature reserves. This study was partially supported by the National University of Singapore (RP960316).
References Andrtn, H., Angelstam, P., 1988. Elevated predation rates as an edge effect in habitat islands: experimental evidence. Ecology 69, 544547. Andrtn, H., Angelstam, P, Lindtrtm, E., Widtn, P., 1985. Differences in predation pressure in relation to habitat fragmentation: an experiment. Oikos 45, 273-277. Angelstam, P., 1986. Predation on ground-nesting birds' nests in relation to predator densities and habitat edge. Oikos 47, 365-373. Blake, J.G., Karr, K.R., 1987. Breeding birds of isolated woodlots: area and habitat relationships. Ecology 68, 1724-1734. Briggs, J.C., 1996. Tropical diversity and conservation. Conserv. Biol. 10, 713-718.
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Brittingham, M.C., Temple, S.A., 1983. Have cowbirds caused forest songbirds to decline? Bioscience 33, 31 35. Brooks, T.M., Pimm, S.L., Collar, N.J., 1997. Deforestation predicts the number of threatened birds in insular southeast Asia. Conserv. Biol. 11,382-394. Burkey, T.V., 1993. Edge effects in seed and egg predation at two neotropical rainforest sites. Biological Conservation 66, 139-143. Chasko, G.G., Gates, J.E., 1982. Avian habitat suitability along a transmission-line corridor in an Oak-Hickory forest region. Wildl. Monogr. 82, 1-41. Corlett, R.T., 1994. What is secondary forest?. Journal Trop. Ecol. 10, 445-447. Corlett, R.T., 1995. Tropical secondary forests. Prog. Physical Geogr. 19, 159-172. Ford, H.A., Davison, G.W.H., 1995. Forest avifauna of Universiti Kebangsaan Malaysia and some other forest remnants in Selangor, Peninsular Malaysia. Malayan Nat. Journal 49, 117-138. Gates, J.E., Gysel, L.W., 1978. Avian nest dispersion and fledging success in field-forest ecotones. Ecology 59, 871 883. George, T.L., 1987. Greater land bird densities on island vs. mainland: relation to nest predation level. Ecology 68, 1393-1400. Gibbs, J.P., 1991. Avian nest predation in tropical wet forest: an experimental study. Oikos 60, 155-161. Hails, C.J., Jarvis, F., 1987. Birds of Singapore. Times Edition, Singapore. Hanski, I.K., Fenske, T.J., Niemi, G.J., 1996. Lack of edge effect in nesting success of breeding birds in managed forest landscapes. Auk 113, 578 585. Hoover, J.P., Brittingham, M.C., Goodrich, L.J., 1995. Effects of forest patch size on nesting success of wood thrushes. Auk 112, 146-155. Hurlbert, S.H., 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187 211. Janzen, D.H., 1978. Predation on eggs on the ground in two Costa Rican forests. Am. Midl. Nat. 100, 467-470. Kroosdma, R.L., 1984. Effect of edge on breeding forest birds species. Wilson Bull. 96, 426-436. Langen, T.A., Bolger, D.T., Case, T.J., 1991. Predation on artificial bird nests in chaparral fragments. Oecologia 86, 395-401. Leimgruber, P., McShea, W,J., Rappole, J.H., 1994. Predation on artificial nests in large forest blocks. Journal Wildl. Manage. 58, 254-260. Lemmon, P.E., 1957. A new instrument for measuring forest overstorey density. Journal Forest. 55, 667-668. Loiselle, B.A., Hoppes, W.G., 1983. Nest predation in insular and mainland lowland rainforest in Panama. Condor 85, 93 95. MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, NJ, USA. Major, R.E., Kendal, C.E., 1996. The contribution of artificial nest experimentsto understanding avian reproductive success: a review of methods and conclusions. Ibis 138, 298-307. Moiler, A.P., 1989. Nest site selection across field-woodland ecotones: the effect of nest predation. Oikos 56, 240 246. Myers, N., 1988. Tropical forests and their species: going, going ...? In: Wilson, E.O., Peter, F.M. (Eds.) Biodiversity. National Academy Press, Washington, DC, pp. 28-35 Nilsson, S.G., Bjtrkman, C., Forslund, P., Htglund, J., 1985. Egg predation in forest bird communities on islands and mainland. Oecologia 66, 511-515. Nour, N., Matthysen, E., Dhondt, A.A., 1993. Artificial nest predation and habitat fragmentation: different trends in birds and mammal predators. Ecography 16, 111-116. Patton, D.R., 1975. A diversity index for quantifying habitat 'edges'. Wildl. Soc. Bull. 3, 171-173. Picman, J., 1988. Experimental study of predation of eggs of groundnesting birds: effects of habitat and nest distribution. Condor 90, 124-131. Ratti~ J.T., Reese, K.P., 1988. Preliminary test of the ecological trap hypothesis. Journal Wildl. Manage. 52, 484-491.
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Ricklefs, R.E., 1969. An analysis of nesting mortality in birds. Smithsonian Contr. Zool. 9, 1-48. Rudnicky, T.C., Hunter, M.L., 1993. Avian nest predation in clearcuts, forests, and edges in a forest-dominated landscape. Journal Wildl. Manage. 57, 358-364. Siegel, S., Castellan, N.J.J., 1988. Nonparametric Statistics for the Behavioural Sciences, 2nd ed. McGraw-Hill, New York. Sieving, K.E., 1992. Nest predation and differential insular extinction among selected forest birds of central Panama. Ecology 73, 23102328. Small, M.F., Hunter, M.L., 1988. Forest fragmentation and avian nest predation in forested landscapes. Oecologia 76, 62-64. Turner, I.M., Corlett, R., 1996. The conservation value of small, isolated fragments of lowland tropical rain forest. Trends Ecol. Evol. 11,330-333. Turner, I.M., Tan, H.T.W., Wee, Y.C., Ibrahim, A.B., Chew, P.T., Corlett, R.T., 1994. A study of plant species extinction in Singapore: lessons for the conservation of tropical biodiversity. Conserv. Biol. 8, 705-712. Vander Haegen, W.M., DeGraaf, R.M., 1996. Predation on artificial nests in forested riparian buffer strips. Journal Wildl. Manage. 60, 542-550. Whelan, C.J., Dilger, M.L., Robson, D., Hallyn, N., Dilger, S., 1994. Effects of olfactory cues on artificial-nest experiments. Auk 111, 945-952.
Whitcomb, R.F., Robbins, C.S., Lynch, J.F., Whitcomb, B.L., Klimkiewicz, M.K., Bystrak, D., 1981. Effects of forest fragmentation on avifauna of the eastern deciduous forest. In: Burgess, R.L., Sharpe, D.M. (Eds.). Forest Island Dynamics in Man-dominated Landscapes. Springer-Verlag, New York, pp. 125-205. Wilcove, D., 1985. Nest predation in forest tracts and the decline of migratory songbirds. Ecology 66, 1211-1214. Willebrand, T., Marcstr6m, V., 1988. On the danger of using dummy nests to study predation. Auk 105, 378-379. Wilson, E.O., 1992. The Diversity of Life. Allen Lane, London. Yahner, R.H., Cypher, B.L., 1987. Effects of nest location on depredation of artificial arboreal nests. Journal Wildl. Manage. 51, 178181. Yahner, R.H., Mahan, C.G., 1996. Effects of egg type on depredation of artificial ground nests. Wilson Bull. 108, 129-136. Yahner, R.H., Scott, D.P., 1988. Effects of forest fragmentation on depredation of artificial nests. Journal Wildl. Manage. 52, 158-161. Yahner, R.H., Voytko, R.A., 1989. Effects of nest-site selection on depredation of artificial nests. Journal Wildl, Manage. 53, 21-25. Yahner, R.H., Wright, A.L., 1985. Depredation on artificial ground nests: effects of edge and age plot. Journal Wildl. Manage. 49, 508513. Yahner, R.H., Morrell, T.E., Rachael, J.S., 1989. Effects of edge contrast on depredation of artificial avian nests. Journal Wildl. Manage. 53, 1135-1138.
ELSEVIER
Biological Conservation 85 (1998) 97-104
Artificial nest and seed predation experiments in tropical lowland rainforest remnants of Singapore Timothy C.M. Wong, Navjot S. Sodhi *, I.M. Turner t School of Biological Sciences, National University of Singapore, Kent Ridge, Singapore 119260, Republic of Singapore Received 16 March 1997; accepted 27 August 1997
Abstract
Tropical lowland rainforests of Southeast Asia are continually being fragmented and lost at an alarming rate. Little is known about the consequences of this large-scale habitat modification. Using artificial nest and seed experiments, we determined predation rates in forest remnants (2.5-1100 ha in area) of Singapore and Pulau Ubin. Singapore (641 km2) is highly urbanised with only 5% of the native forest cover remaining, whereas Pulau Ubin (11 km2) is relatively less developed with about 60% of the native forest cover remaining. We specifically determined if predation rates varied in relation to: (i) distance from edge, (ii) forest types, (iii) forest areas, (iv) isolation, (v) edge to area ratio, (vi) canopy closure, and/or (vii) area (Singapore vs Pulau Ubin). Overall, 80.5% (n = 328) of artificial ground nests were depredated, of which 55.3% were predated by small mammals. For seeds, 98.2% (n = 219) experimental stations were predated. Generally, the predation rate did not vary significantly in relation to the distance from the edge, though a primary forest remnant had lower artificial nest and seed predation rates than the other remnants. Pulau Ubin remnants were found to have lower predation rates than remnants on Singapore island. No significant correlations were found between predation rates and remnant area, isolation from other remnants, or the edge/area ratio, or canopy density. Relatively high predation rates in some tropical secondary and primary forest remnants may greatly influence plant regeneration and bird community structure. © 1998 Elsevier Science Ltd. All rights reserved Keywords." Fragmentation; Negative edge effects; Nest predation; Seed predation
I. Introduction
Due to human activities (e.g. agriculture and settlements), large forest tracts are continually being fragmented into smaller patches. Forest fragmentation and loss can have deleterious consequences for the native biota (Whitcomb et al., 1981). Because it results in greater edge (Hoover et al., 1995), generalized predators that are adapted to edge habitats can more easily penetrate forest remnants than similar continuous forests (Whitcomb et al., 1981; Wilcove, 1985). Documentation of high predation rates in forest remnants is thus important from a conservation perspective as such a phenomenon can have dire consequences for avian reproductive success and seedling establishment (Burkey, 1993). Because actual predation events are hard to observe, one indirect way to determine how well bird and plant species may be reproducing in fragments is through * Corresponding author. Fax: + 65-874-2486; e-mail: [email protected] t Present address: Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA. 0006-3207/98/$19.00 © 1998 Elsevier Science Ltd. All rights reserved PII: S0006-3207(97)00145-6
artificial nest and seed predation experiments. The nest and possibly seed predation in forest patches may depend on a number of factors including patch size, distance from edge, and/or habitat age and structure (Gates and Gysel, 1978; Chasko and Gates, 1982; Wilcove, 1985; Yahner and Wright, 1985; Andr~n and Angelstam, 1988; Picman, 1988). From a conservation perspective, it also is important to identify the factors that may influence predation rates in forest remnants. Despite alarming rates of forest loss and fragmentation in the tropics (Myers, 1988; Turner and Corlett, 1996), few studies have examined nest predation in fragmented tropical landscapes (e.g. Gibbs, 1991; Sieving, 1992; Loiselle and Hoppes, 1983). To our knowledge, no nest predation experiment has been conducted in the tropical lowland rainforests of Southeast Asia. It is therefore unknown if studies done in other regions can be applicable to this region. Apart from Burkey, 1993, no work on seed predation in relation to forest fragmentation within the tropics has been published. We experimentally tested whether the predation rate of nests and seeds are affected by (i) distance from edge,
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(ii) forest types, (iii) size of fragment, (iv) isolation, (v) edge to area ratio, and/or (vi) canopy closure. Also, we compared the predation rates between the main island of Singapore and those at another island, Pulau Ubin. We hope that with our study, the knowledge gained may influence decisions regarding forest harvesting practices within tropical rainforests of Southeast Asia.
2. Methods and materials 2.1. Study sites
We used eight forest fragments on two islands. Five study sites were on Singapore (area=641 kmZ), while the other three sites were on Pulau Ubin (11 kmZ). The native forested area of Singapore (103°50'E, l°20'N) and Pulau Ubin (103°57'E, 1°25'N) is about 5 and 60%, respectively (Turner et al., 1994). Singapore is one of the most densely populated areas, whereas Pulau Ubin is relatively little developed. The five study sites in Singapore included two primary forests (MacRitchie, Bukit Timah 1), two secondary forests (Bukit Timah 2, Central Catchment), and one abandoned rubber plantation (Teck Chong). The fragment, Bukit Timah Nature Reserve (Bukit Timah 2) is actually the secondary forest surrounding another study site, Bukit Timah 1, which is a primary forest. Of the three sites on Pulau Ubin, one was a secondary forest (Ubin 3) whereas the other two sites were abandoned rubber plantations (Ubin 1 and Ubin 2). The study fragments were surrounded by a variety of edges such as track, road, reservoir, and pipeline. The primary forest is defined as a remnant where the original forest cover is still present (Corlett, 1995), and where there are many large primary forest trees present, such as dipterocarps. Secondary forest is defined as the regrowth from disturbed primary forest where the break in continuity is still detectable in the structure and/or floristic composition of the vegetation (Corlett, 1994). The rubber plantation sites in this study were actually secondary forests (according to the above definition). But they were treated as rubber plantation sites because most of the trees found in these plots were rubber trees (Hevea brasiliensis). Forest remnants are defined as forested areas surrounded by unforested habitat on all sides. In this study, forest remnants, patches, sites, and fragments are used interchangeably. 2.2. Materials
For the nest predation experiment, chicken eggs were used. The use of chicken eggs served to simulate the eggs of the Red Jungle Fowl (Gallus gallus), a groundnesting bird which occurs in Pulau Ubin (pers. obs.). As suggested by both Janzen, 1978 and Whelan et al., 1994,
fresh chicken eggs (bought on the same day of experiment set-up) were used. Raw shelled peanuts were used for the seed predation studies. The use of peanuts served as the introduction of an 'exotic seed', thus giving estimates of predation rates that are from generalists, rather than specialist predators (Burkey, 1993). In addition to real eggs and seeds, plasticine eggs and peanuts, were also used. Plasticine was used to determine the type of predators that attacked the eggs and seeds by the bite-marks left on the plasticine (cf. Moiler, 1989; Langen et al., 1991). The imitation eggs and peanuts were hand-made from brown plasticine. The plasticine chicken eggs were then painted with poster colours to give a 'chicken-egg' colour. During the handling of the real and plasticine eggs and peanuts, rubber gloves were worn at all times to the reduce contamination with human scent. However, because of their smell, it is possible that painted plasticine eggs may have influenced the behaviour of certain types of predators. 2.3. Methods
Within each transect, there usually were five experimental stations. The number of transects at site A, B l, B2, C, D, E, F, G and H were 15, 5, 10, 15, 20, 16, 15, 15, and 10, respectively (Table 1). Each transect started from the edge of the forest (here defined as the first tree or shrub) and ran 100m into the forest, and each transect was arranged perpendicular to the edge. The five stations were demarcated at 0 (the edge), 25, 50, 75, and 100m. The egg experimental stations were located at the 0, 50, and 100m positions whereas the seed experimental stations were placed at the 25 and 75 m marks. At an egg experimental station, we placed one real chicken egg and one plasticine egg. At each seed experimental station, we placed five raw peanuts and five plasticine peanuts. All peanuts were placed in a petri-dish. Minimal markings were placed along the transect to avoid giving cues to potential predators. The experimental stations (eggs or peanuts) were placed at random distances (1-5m) and at random directions (left or right) of an experimental station. To facilitate relocation, they were usually placed near buttresses of trees or the base of larger saplings, as done by many previous researchers (e.g. Yahner et al., 1989; Gibbs, 1991; Rudnicky and Hunter, 1993; Vander Haegen and Degraaf, 1996; Yahner and Mahan, 1996). We attempted to cover the eggs and seeds by adjusting the vegetation, such that when viewed directly from above, at a height of 1.8 m, the percentage cover directly above the seeds and eggs was about 50%. The eggs were placed on the open ground and no attempt was made to create any artificial nests. Although no attempt was made to construct an artificial nest, we designate the egg experiment stations as nests because many ground nesting bird
T.C.M. Wong et al./Biological Conservation 85 (1998) 97-104
Table 1 Results of artificial nests predation rates, small mammal predation rates, and seed predation rates for all remnants. Figures in parentheses are number of experimental stations preyed over the total number of experimental stations Site
A B1 B2 C D E F G Total
H
Predation rates Nest
Small mammals
Seed
86.05% (37/43) 93.33% (14/15) 76.67% (23/30) 64.44% (29/45) 80.00% (48/60) 68.89% (31/45) 91.11% (41/45) 91.11% (41/45)
72.97% (27/37) 42.86% (6/14) 78.26% (18/23) 48.28% (14/29) 70.83% (34/48) 2%03% (9/31) 26.83% (11/41) 65.85% (27/41)
100.00% (30/30) 100,00% (10/10) 100.00% (20/20) 93.33% (28/30) 100.00% (40/40) 96.77% (30/31) 100.00% (28/28) 96.67% (29/30)
80-49% (264/328)
55.30% (146/264)
98.17% (215/219)
73.33% (44/60)
29.55% (13/44)
100.00% (60/60)
Site A: Teck Chong rubber plantation (area=35ha, edge/area ratio = 2-38, isolation = 250 m, canopy density= 88.2%). Site Bh Pulau Ubin rubber plantation I (Ubin 1) (2.5ha, 2.32, 240m, 83.3%). Site B2: Pulau Ubin rubber plantation 2 (Ubin 2) (170 ha, 1.30, 300 m, 88.6%). Site C: Pulau Ubin secondary forest (Ubin 3) (100ha, 2.26, 300m, 80.3%). Site D: Central Catchment (secondary forest) (ll00ha, 2.72, 420m, 90.2%). Site E: MacRitchie Reservoir Park (primary forest) (65ha, 2.10, 300 m, 94.9%). Site F: Bukit Timah Nature Reserve (primary forest) (Bukit Timah 1) (164 ha, 1-65, 620 m, 80.9%). Site G: Bukit Timah Nature Reserve (secondary forest) (Bukit Timah 2) (164 ha, 1.65, 620 m, 85-6%). Site H: Central Catchment (secondary forest); same as the site D but transect lengths in this experiment were extended up to 250 m into the forest.
species do not build elaborate nests. To minimize the possibility of attracting the attention of potential predators, we minimized the time spent at each station. The transects within a fragment were spaced 5 0 m away from each other (cf. Gibbs, 1991). Paths were not cleared along the transects and every effort was made to minimize the impact of setting up the experiment. The experiments were performed in August 1996, which is during the end of the birds' breeding season in Singapore (Hails and Jarvis, 1987). To avoid pseudoreplica-
99
tion (Hurlbert, 1984), we conducted experiments only once at each site except one site (site D) where during a subsequent experiment, we extended the transects up to 250 m (see below). To determine the predation rates, experimental nest and peanut stations were checked on day 8, except for the site Ubin 2, which was checked on day 10. Nests were considered as preyed upon if: (i) an egg was missing, (ii) there were cracks or peck marks on the real chicken egg, (iii) the chicken egg was smashed, or (iv) bite-marks were on the plasticine eggs. Similarly, for the peanuts, the station was considered preyed upon if: (i) any of the peanuts were missing, or (ii) there were bitemarks observed on the plasticine peanuts. During the setting up and checking days, all sightings of potential predators (e.g, Corvus spp.) were recorded. Predation by small m a m m a l s was determined by examining the bite marks imprinted on the plasticine eggs and comparing these to teeth sizes of potential predators. The teeth sizes of potential predators were obtained from material in the Zoological Reference Collection, National University of Singapore. If a plasticine egg had incisor marks <2 m m wide, we considered it being predated by a small mammal. Incisor marks > 2 m m wide on plasticine eggs were considered to be predation by larger-sized mammals, Predation by avian predators was determined by the presence of beak marks on plasticine eggs. Similarly, other specific markings on plasticine eggs revealed predation by other predators such as reptiles. Because 100 m within the forest may still be considered as an edge (Kroosdma, 1984), we further performed an experiment in a fragment (Central Catchment) where the transect lengths were extended up to 250 m into the forest. The experimental stations were located at 0, 50, 100, 150, 200, and 250m. At each distance, both eggs and seeds were placed. The direction (left or right) in which the eggs or seeds were placed was determined randomly. The distance between neighbouring transects was 50 m. 2.4. M e a s u r e m e n t s o f variables
As suggested by Small and Hunter (1988), aerial photographs and topographical maps were used to determine the area and the edge length of each site. The fragment areas were determined by using an area measuring machine (Area Measurement System, DeltaT Devices Limited, UK). Edge/area index (SI) was obtained by measuring the perimeter of the fragment on the topographical m a p with a curvimeter, and substituting the values into the equation formulated by Patton (1975),
Edge/area index = circumference - x/(2 x zr × area)
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Isolation index was obtained by measuring the distance of the nearest forest plots (>4 ha in area) in the northern, eastern, southern, and western directions. These were averaged to give the isolation index (li) (Blake and Karr, 1987). Canopy density was also measured by using a spherical densiometer (Model A). At each distance demarcation of the transects, canopy density readings were taken in the four cardinal directions, and the canopy density for the experimental station was obtained by calculating the mean of these four readings (Lemmon, 1957).
2.5. Statistical analyses Non-parametric analysis of variance (Kruskal-Wallis ANOVA) was used to test whether transects within each site were significantly different from each other in terms of predation rates (Siegel and Castellan, 1988). The effect of distance from the edge on the predation rate was tested using the Kruskal-Wallis ANOVA for the eggs, and Mann-Whitney U test for the peanuts. G-statistic tests were used to determined if there were significant differences in predation rates among fragments with different sizes, and habitat types. Spearman-Rank Correlations were used to determine if there were any significant correlations between predation rates and canopy density, area of the fragment, isolation, or edge/ area ratio. Spearman-Rank Correlations were also used to detect for correlations between nest and seed predation rates. All statistical tests were conducted using STATVIEW. Significance level for all statistical tests was set at 0.05. Throughout the text, i refers to standard error.
detected for any of the fragments. Thus, this allowed the data from each fragment to be pooled for further analyses. No significant differences (ANOVAs, p > 0.16) were detected in nest predation rates relative to the distance from the edge for any of the fragments. The nest predation rate differed significantly among fragments (G = 20.667, d.f. = 7, p = 0.01; Table 1). There was also a significant difference in the nest predation rate among Singapore fragments (p = 0.02, Tables 1 and 2). A significant difference in nest predation rates was detected between the two primary forest fragments (/9=0.01, Table 2). Further analysis showed that MacRitchie (site E) had the lowest nest predation rate (P= 0.01) among the fragments on Singapore (Table 1). There was no significant difference in the nest predation rate among forest types for Pulau Ubin (p = 0.08, Table 2). Thus, these were pooled and compared with the Singapore fragments. There was a significantly higher (p=0-01) predation rate in Singapore (sites A + D + G ; mean predation rate=85.7+3.3%) than Pulau Ubin fragments ( B I + B 2 + C ; 78.1+8.5%) (Table 2).
3.2. Nest predation by small mammals Predation by small mammals was analysed to determine the intensity of small mammalian predation on eggs. No significant differences in small mammal predation rates were detected among transects within each fragment (ANOVAs, p > 0-26). Significantly different small mammal predation rates were detected among fragments (G=40.819, d.f.--7, p=0.01; Table 1). Small mammal predation rates also differed in relation to the Table 2 G-tests for difference in nest predation rates among forest types
3. Results
Site
Predation of artificial nests and seeds was observed at all sites (Table 1). Overall, 80-5% of the artificial nests were preyed upon, out of which 55.3% were preyed upon by small mammalian predators, and the rest by medium-sized mammals, birds, and monitor lizards (Varanus salvator). For seeds, 98.2% of the stations were preyed upon, with five fragments registering 100% predation rates (Table 1). Potential nest and/or seed predators observed at various sites include monitor lizard, crows, squirrels (Sundasciurus tenuis and Callosciurus notatus), wild pig (Sus scrofa), feral dog (Canis spp.), banded leaf monkey (Presbytis femoralis), and long-tailed macaque (Macaca fascicularis).
Singapore fragments All Primary Secondary Secondary (p) vs rubber Secondary (p) + rubber vs primary (Site E) Secondary (p) + rubber vs primary (Site F)
3.1. Nest depredation No significant differences (Kruskal-Wallis ANOVAs, p>0-10) in nest predation rates among transects were
Pulau Ubin fragments All Singapore and Pulau Ubin fragments Mainland-secondary (p) + rubber vs Ubin-secondary + rubber (p) Primary (Site E) against all other sites
G
d.f.
p
11.31 6.94 2.46 0.04 6.00 1.06
4 1 1 1 1 1
0.02* 0.01" 0.12 0.84 0.01" 0.30
5-06 2 0,08 7.36
1 0.01"
10.38 1 0.01"
Primary, Primary forests (Site E and Site F). Secondary, Secondary forests (Site C, Site D and Site G). Rubber, Rubber plantations (Site A, Site BI and Site B2). For site abbreviations, see Table 1. (p), Pooled data. * Significance at ~ = 0.05.
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distance from the edge for only two fragments (Table 3). Both sites A (of mammalian predation on 27 nests, 12, 8, and 7 nests were predated at 0, 50, and 100m, respectively) and B2 (of mammalian predation at 18 nests, 8, 6, and 4 were predated at 0, 50, and 100m, respectively) had the highest nest predation rates by mammals at 0 m and the lowest nest predation rates by mammals at 100m, with intermediate nest predation rates at 50 m. Small mammal nest predation rates differed significantly among forest types in Singapore fragments (p=0.01, Tables 1 and 4). Primary forests had significantly lower small mammal predation rates than all other forest types in Singapore (p=0.01, Tables 1 and 4). Significant differences in small mammal predation rates were also found for forest types in Pulau Ubin (p=0-03, Table 4). The rubber plantations exhibited significant differences in small mammal predation between the two fragments in Pulau Ubin (p=0.02). The fragment B2 had significantly higher small mammal predation rate than the other two sites on Pulau Ubin (Table 1). When Singapore sites (those that had no significant difference in small mammal predation rates, A+D+G; mean predation r a t e = 7 1 - 9 + l . 5 % ) were compared with Pulau Ubin sites (B1 + C ; 42.9+ 1.1%), higher predation was detected for Singapore sites (p=O.O1). 3.3. S e e d predation
No significant differences were detected among transects in seed predation rates within all fragments (ANOVAs, p > 0.45). Also, distance from the edge did not affect seed predation (Mann-Whitney U-tests, p > 0.15). The seed predation did not differ significantly among fragments ( G - 7 - 0 1 9 , d.f.=7, p=0.43; Table 1). Because of no significant variations in seed predation rates among fragments, further analyses were not carried out, bearing in mind that all the sites had similar predation rates (Table 1). Table 3 Kruskal-Wallis ANOVAs (KW) for difference in small mammal predation rates in relation to the distance from the edge Site
KW
d.f.
p
A B1 B2 C D E F G
5-91 1.63 5.94 O.44 0-48 3-55 0.50 4.03
2 2 2 2 2 2 2 2
0.05* 0.44 0.05* O-80 0.79 0.17 0.78 0-13
For site abbreviations, see Table 1. * Significanceat a = 0.05.
Table 4 G-tests for differencein small mammal nest predation rates among forest types Site
Singapore fragments All Primary Secondary Secondary (p) vs rubber Secondary (p) + rubber vs primary (p) Pulau Ubin fragments All Rubber Rubber (BI) vs secondary Rubber (B2) vs secondary Mainland-secondary (p)+rubber vs Ubin- secondary+ rubber (B1)
G
d.f.
p
33.16 0.04 0.25 0.25 33.70
4 1 1 I 1
0.01" 0-84 0.61 0.62 0-01"
7.20 5.85 0.19 5.66
2 1 1 1
0.03° 0.02" 0.66 0.02*
7.36 1 0.01"
* Significanceat a = 0.05.
N o significant correlation was found in nest and seed predation rates (rs=0.47, d.f.=8, p=0.22; Table 1). Also, no significant correlation between small mammal predation rates and seed predation was found (rs = 0.22, d.f. = 8, p = 0.56; Table 1). For extended transects, there were no significant differences among transects for nest predation rates ( K W = 15.42, d.f. = 9, p = 0.08), small mammal nest predation rates ( K W = 9.82, d.f. = 2, p = 0.37) and seed predation rates (KW=0.00, d.f. = 9, p = 1.00). Predation rate (nest, small mammal, or seed) differences in relation to the distance from the edge were also not detected (ANOVAs, p > 0-46). 3.4. Patch characteristics and predation rates
No significant correlations were found between predation rates (nest predation, small mammal predation, and seed predation) and the four variables (fragment area, edge/area ratio, isolation index, and canopy density) (all Spearman rank correlations, n =8, p > 0 . 3 3 ) (Table 1).
4. D i s c u s s i o n
Our results show that the predation rate on artificial nests and seeds is relatively high in tropical rainforest remnants of Singapore and Pulau Ubin than reported from similar studies elsewhere (e.g. Yahner and Wright, 1985; Andr6n and Angelstam, 1988; Gibbs, 1991; Burkey, 1993). The unusually high predation rates in Singapore and Pulau Ubin could be due to several reasons. First, matrix (area surrounding remnants) is highly urbanised, at least, in Singapore. Urban areas can harbour relatively high densities of potential
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predators such as feral animals (e.g. dogs) and corvids. Second, Singapore is one of the highly fragmented landscapes with only 5% of the native forest cover remaining. This may have resulted in many potential predators (e.g. monkeys) being confined only to remaining pockets of forests. Last, it is possible that our experiment design (using of artificial painted eggs) may have resulted in high levels of predation of artificial nests. Singapore remnants usually revealed higher nest predation rates than those at Pulau Ubin. Nest predation rates on islands are usually higher than those at comparable mainland sites (Loiselle and Hoppes, 1983; Nilsson et al., 1985), which is attributed to the high density of small to medium-sized predators on islands. However, our study shows that predation rates may differ among different islands. The lower predation rates in Pulau Ubin could be due to several factors such as higher native forest cover than Singapore and it is still less developed, both of which may have resulted in lesser influx of generalist feral predators (e.g. feral dogs) and human associated predators (e.g. corvids) there. Or it may be due to the notion that smaller islands have lower species diversity (including predators) and abundance than larger islands (MacArthur and Wilson, 1967). We found the variation in nest predation rates among some of our remnants. However, the patch variables that we measured (remnant area, isolation, edge/area ratio, and canopy density) failed to reveal significant correlations with predation rates. Different studies have attributed correlations of artificial nest predation rates with different variables such as canopy density, area, isolation, vegetation, and edge/area ratio (e,g. Burkey, 1993; Major and Kendal, 1996). The lack of a correlation between predation rates and various patch variables in our study can be due to the variables that we did not measure (e.g. density and abundance of potential predators), which may more strongly affect the predation rates. We found most cases of nest predation by mammals (all sizes combined; 71.9%), with only 6.1% nest predation attributed to avian predators. This is different from a number of previous studies which reported high avian predation of artificial nests (Andrrn et al., 1985; Angelstam, 1986). One reason for the high mammalian nest predation in Singapore could be due to the habitat surrounding the edge. In several similar studies in temperate regions, the edge consisted of pasture lands or farmlands (Yahner and Wright, 1985; Yahner and Cypher, 1987). Corvids are usually abundant in such edges as they either scavenge for food in the farmlands, or they may search for nests in the pasture or forested areas. In Singapore, isolated forests are usually surrounded by urbanised areas. Corvids can be abundant in urban areas, but in Singapore, they are considered as pests and are controlled by the Primary Production
Department of Singapore by regular shooting. Artificial predation rates have been found to be higher at edges than forest interior in several studies (Gates and Gysel, 1978; Brittingham and Temple, 1983; Wilcove, 1985; Burkey, 1993). Distance effects (higher predation rates at forest edge vs forest interior) were usually attributed to the increase in potential nest predators along the edge (Andrrn and Angelstam, 1988). Such potential nest predators include corvids as well as mammals (Yahner and Scott, 1988; Yahner and Voytko, 1989). In contrast, however, there are also a number of studies the results of which do not support higher predation rates at edges than forest interior (Angelstam, 1986; Ratti and Reese, 1988; Small and Hunter, 1988; Nour et al., 1993; Hanski et al., 1996). It has also been suggested that at edges, there is higher predation by avian predators than in forest interiors. However, this may be compensated for by a rise in mammalian predation because in a heavily fragmented landscape, such as Singapore, forest-dwelling mammals may be confined to forest fragments. Thus, the net effect was that predation rates remained relatively constant, and thus, no distance effect was detected in most cases, even for the experiments with transect lengths of 250 m. No significant correlation was found between nest and seed predation rates, even though there was a high correlation coefficient for nest and seed predation rates (rs--0.47). This could probably be due to the small sample size. It would therefore seems to be reasonable to expect a high predation rate for nests if there was a high predation rate for seeds, since both nests and seeds were exposed to similar types of predators. Also, no significant correlation was found between small mammal nest predation and seed predation rates, which again may be an artefact of small sample size. 4.1. Implications and limitations Southeast Asia is considered to be a one of the megabiodiversity regions (Briggs, 1996). However, deforestation in this region is predicted to cause mass species extinctions (Wilson, 1992; Brooks et al., 1997). Despite this, rainforests in Southeast Asia are continually being cleared and fragmented at an alarming rate (Turner and Corlett, 1996) and there appears to be no clear guidelines for reserve area and cut-block designs. Artificial and natural predation rates may differ (Willebrand and Marcstr6m, 1988). Because our study is only based on artificial predation rates, it is not known to what extend our study is indicative of natural predation rates. Experiments, such as ours, likely determine predation pressure by generalist predators and thus are suitable for community-level nest/seed vulnerability (Sieving, 1992) and at best only provide an estimation of relative predation rates (Loiselle and Hoppes, 1983; Wilcove, 1985).
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Our study also is done in one of the highly urbanised landscapes (Singapore), therefore, it is not known how applicable our study will to other forested landscapes in the region. However keeping the above limitations in mind, some postulations/recommendations can be derived from our study. First, many forest flora and fauna have already gone extinct within Singapore (Turner and Corlett, 1996). It is possible that relatively high level of predation rates because of high level of fragmentation may be one of the factors influencing the extinctions of certain forest flora and fauna from Singapore. Second, considering that high predation rates were observed in remnants as large as l l00ha and in those that were relatively less disturbed (primary forests, Table 1), there is an urgent need for studies similar to ours from various landscapes and forest types of Southeast Asia. Data from these studies can then be used by local conservation and government agencies to critically examine forest harvesting practices within Southeast Asia. In this study, we have been dealing with ground nests. Experiments should be carried out on studies with domed and pouch nests, which provide more protection and concealment from predators than open-cup nests (Ricklefs, 1969), and are more common among tropical, forest breeding birds (Ricklefs, 1969; Gibbs, 1991). Nests of tropical birds may also be more dispersed temporally than nests in temperate forests because the breeding seasons of tropical, wet forest birds are longer, extending over much of the year (Gibbs, 1991). Thus, temporal artificial nest predation studies may reveal certain yet unknown trends.
Acknowledgements The authors thank Dr. Hugh Tan, Mr. Tommy Tan, Benjamin Lee, and Janet Nichol for help. They are grateful to the National Parks Board of Singapore for permission to carry out research in nature reserves. This study was partially supported by the National University of Singapore (RP960316).
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