BIOTROPICA 36(2): 156±164 2004

Alien Abduction: Disruption of Native -Pollinator Interactions by Invasive Species1

Jaboury Ghazoul 2 Department of Environmental Science and Technology, Imperial College London, Silwood Park, Ascot, Berks SL5 7PY, UK

ABSTRACT The indirect impacts of Shorea siamensis-logging on the reproductive ecology of Dipterocarpus obtusifolius, a self- incompatible butterfly-, moth-, and bird-pollinated tree, were studied in tropical dry forest in Thailand. Pollinator activity at D. obtusifolius trees and subsequent seed production were recorded in three forest areas subject to differing intensities of S. siamensis extraction. The pollinator and plant understory communities in these areas were also noted. Forest areas subject to high S. siamensis extraction intensities had very high understory flowering plant cover, dominated by the exotic invader Chromolaena odorata. Activity of butterfly pollinators at D. obtusifolius trees decreased in these disturbed areas, although their abundance remained comparable to other forest areas subject to only moderate or no extraction. For sphingid moth pollinators, there was no difference across differentially disturbed forest areas in either abundance or in the proportion bearing pollen. Pollinator activity by birds increased at highly disturbed locations but was not sufficient to offset a decline in overall pollinator activity at D. obtusifolius canopies in areas of heavy S. siamensis extraction. Thus, extraction of S. siamensis indirectly affected the pollination of D. obtusifolius, primarily by causing changes in the foraging behavior of butterfly pollinators rather than their abundance. A shift in the relative abundance of floral nectar resources from the canopy to the understory, a consequence of S. siamensis extraction and invasion by C. odorata, led to a parallel shift in foraging location of the principal diurnal pollinators, the butterflies, toward the understory. Despite reduced pollination at disturbed sites, behavioral changes did not translate into a D. obtusifolius seed set effect, possibly because pollination by birds (or moths) at the disturbed site compensated for reduced butterfly pollination. ECTION

S Key words: compensation; Dipterocarpaceae; disturbance; invasive ; pollination; reproductive success, seed set; tropical dry forest.

PECIAL TROPICAL TREES ARE MOSTLY SELF-INCOMPATIBLE and caused by disturbance may lead to the restructuring

S generally dependent on -mediated pollina- of the plant–pollinator interaction web. tion for seed production (Bawa 1974, 1990). Dis- In Thailand, selective extraction of the forest turbances that impact animal vectors of pollen tree Shorea siamensis (Dipterocarpaceae) reduces its transfer may therefore affect the reproductive out- local density, causing a decline in its effective pol- put of tropical trees. Pollination processes can be lination and reproductive output (Ghazoul et al. disrupted by declining pollinator abundance 1998). Although S. siamensis is not tightly linked (Rathcke 2000), changes in resource availability to other organisms through strong mutualistic in- (Jennersten 1988), the spatial distribution of floral teractions, as a common forest tree it is likely to resources (Ghazoul et al. 1998), or competitive ex- support numerous weak community interactions. clusion from floral resources by inefficient polli- It is therefore possible that extraction of S. siamensis nating species (Huryn 1997). The majority of pol- could indirectly affect the reproductive ecology of linator interactions, however, are generalist in that other trees that share its Trigona bee pollinators, or several or many invertebrate protagonists may be less obviously, by causing changes that af- involved. While this provides insurance against the fect the foraging behavior or abundance of other loss or decline of a mutualistic partner, fidelity pollinating . Such habitat changes may in- among partners is not assured. Consequently, the clude invasion of a disturbed forest habitat by alien dynamic nature of most plant–pollinator interac- plant species that alter the abundance and distri- tions may be a function of the relative abundance bution of floral resources in the forest landscape, of floral resources, and shifting plant abundances possibly leading to changes in the behavior of pol- linators in that landscape (Chittka & Schurkens 1 Received 30 October 2003; revision accepted 12 Feb- ruary 2004. 2001). In this study, I investigated how extraction 2 E-mail: [email protected]; Fax: ϩ(0)20 7594 of S. siamensis results in changes in habitat struc- 2308. ture and composition, particularly in terms of in-

156 Indirect Effects on Pollination 157 vasion of the forest understory by an alien plant within the park boundary, has been subject to the Chromolaena odorata, and how this in turn affects same strict controls as the undisturbed sites. Tree the reproductive ecology of Dipterocarpus obtusifo- densities averaged 101 Ϯ 10/ha (x¯ Ϯ SE, N ϭ 20). lius, a common sympatric dipterocarp tree. The Observations were made through the entire extent specific aims of this study were to compare (1) un- of moderately disturbed forest, which covered an derstory plant composition, (2) abundance of lep- area of ca 15 km2. idopteran pollinators of D. obtusifolius, (3) polli- Highly disturbed forest exists in a 3–5 km wide nator activity at D. obtusifolius trees, and (4) repro- buffer zone that extends along the length of the ductive output of D. obtusifolius across three sites northeastern boundary of the sanctuary for ca 15 differing in intensity of S. siamensis extraction. km. Prior to the designation of the buffer zone in 1990, this area was subject to widespread extrac- METHODS tion of S. siamensis that resulted in the currently low total tree densities of 73 Ϯ 8/ha (x¯ Ϯ SE, N SPECIES AND STUDY SITES. Dry deciduous forests ϭ 20). Disturbed (D) study sites were within a 10 (DDF) in Thailand are dominated by four tree spe- km2 area within this buffer zone. cies belonging to two genera, Shorea and Diptero- All sites were located within the same forest carpus (Dipterocarpaceae). Prior to a national log- basin and had similar elevations and topography. ging ban in 1989, S. siamensis Miq. and S. obtusa The soil is homogeneous throughout the basin, Wall. ex Bl. were extracted commercially from with no apparent major differences between sites many forests, leaving D. tuberculatus Roxb. and D. in soil depth, pH, organic content, or water, nitro- obtusifolius Teijsm. intact. Since then, illegal small- gen, potassium, and phosphorous availability (Gha- scale extraction of Shorea (mostly for domestic use) zoul, pers. obs.). Grazing and small-wood collec- S has continued. The resulting degraded forests have tion are prohibited in the sanctuary but limited PECIAL reduced densities of Shorea but not Dipterocarpus. grazing by cattle is permitted in the buffer zone. This study, conducted from October 1997 to An efficient system of fire control and prevention April 1998, used DDF areas of differing distur- had been established by park authorities, such that bance intensity at Huay Kha Khaeng Wildlife the most recent major fire occurred five years be- S Sanctuary, Uthai Thani Province, western Thailand fore the start of the work and this had affected all ECTION (15Њ36ЈN, 99Њ20ЈE). Huay Kha Khaeng (HKK) three study areas. Indeed, selection of areas for has a total area of 2575 km2; 381 km2 is DDF, study was constrained by the need to find areas most of which occurs in a single 260 km2 block with similar disturbance histories other than log- on the eastern edge of the sanctuary (Nakhasathien ging. & Stewart-Cox 1990) where this work was con- At Huay Kha Khaeng, D. obtusifolius produces ducted. Anthropogenic disturbance over two de- its large funnel-shaped flowers annually from Oc- cades has created a gradient of decreasing distur- tober to January. The self-incompatible flowers are bance intensity from the edge of the sanctuary to produced alternately on panicles and are pollinated its interior. Three areas were selected to represent by butterflies, moths, and, occasionally, birds (Gha- this gradient. zoul 1997). In common with many other trees in Three undisturbed sites (labeled collectively as this forest type, D. obtusifolius is deciduous and is U) were located in a 3 x 6 km area within the leafless from November to late January or early much larger ‘‘undisturbed’’ forest region where hu- February. The deciduous nature of this tree and the man interference is strictly prohibited and ade- forest generally, together with its modest height of quately enforced. Tree (Ͼ10 cm diameter at breast between 15 to 25 m, allowed for easy observation height [DBH]) density in this area averaged 117 Ϯ of flower and fruit production and pollinator ac- 8/ha (x¯ Ϯ SE, N ϭ 20; Ghazoul et al. 1998). Un- tivity. disturbed forest extended from ca 9 km within the sanctuary boundary to its interior and research SITE VEGETATION CHARACTERISTICS. To estimate plots were located in a region 14–20 km within changes in the composition of the forest understory the sanctuary boundary. following removal of S. siamensis trees, understory In moderately disturbed forest areas (M), and flowering plant cover and species richness were re- prior to the relocation of villages outside the sanc- corded in 6 m radius plots (113 m2) at the start, tuary in 1990, Shorea trees had been extracted in middle, and end of each butterfly census transect small numbers (full details given in Ghazoul et al. (described below). Each flower-bearing plant spe- 1998). Since then this region, located 3–9 km cies was given a percent cover estimate by taking 158 Ghazoul

the mean of independent estimates made by two 12V car battery to the top edge of the sheet. Light observers. Summing percent cover across all species trapping was conducted at the center of each of 12 gave total flowering plant cover in each plot. It was butterfly transects (see below) in the three forest not possible to identify all species, but each was regions. Two sets of light-trapping equipment per- allocated a unique code and samples were taken to mitted two transects to be sampled simultaneously, confirm identities at other locations. and these were selected randomly from the total set until 12 transects per site had been completed. POLLINATOR ACTIVITY. The large pendant D. ob- Light trapping was only carried out on relatively tusifolius flowers are pollinated by moths, butter- dark nights (i.e., from waning to waxing half- flies, and birds. Anthesis occurs at ca 2000 h and moons) and from 2100 to 2400 h continuously. stigmatic surfaces remain receptive, and pollen vi- Sphingid moths attracted to the light were caught able, to noon on the following day (Ghazoul with a hand net and transferred to transparent plas- 1997). Nectar secretion begins about one hour af- tic boxes lined with tissue paper to which some ter anthesis and continues to early afternoon on the drops of ethyl-acetate had been applied. Dead following day. Full details of the pollination biol- moths were transferred into paper envelopes and ogy of D. obtusifolius are found in Ghazoul (1997). labeled. Tissue paper was replaced and fresh ethyl- Using binoculars (Leica 8 x 32 and 10 x 42) and acetate was applied after each capture. The pro- a field telescope (Nikon 25–56x magnification), the portion of moths carrying D. obtusifolius pollen was activities of butterfly and bird pollinators were re- determined using a binocular microscope. corded by noting their abundance in D. obtusifolius canopies at each of the three study sites. The num- POLLINATOR ABUNDANCE. Butterfly pol- ber and species identity of flower visitors in D. ob- linators of D. obtusifolius were surveyed for 30 min- tusifolius crowns were recorded during one-minute utes along each of 20 transects (500 m) at each observation periods at ten-minute intervals. Obser- site. Each transect was surveyed only once. Tran- vations at each tree were continued for three hours sects were located as far as possible from existing ECTION between 0830 and 1200 h, overlapping the period tracks and paths. Within a site, transects were S of stigma receptivity, and for 30 trees at each site. mostly parallel to each other and adjacent transects To maximize independence of data, distances be- were separated by at least 200 m and up to ca 600 tween neighboring observation trees were at least m. Two observers recorded butterflies within an es- 220 m. Each tree was used only once. Observations timated 20 m each side of the transect. Binoculars PECIAL were undertaken from 21 October 1997 to 6 Jan- aided identification and care was taken to avoid S uary 1998, coinciding with the peak D. obtusifolius counting the same butterfly twice. Species were flowering season. Weather conditions remained dry identified using Pinratana (1979, 1983, 1988) and and sunny throughout this period. Pinratana and Eliot (1992). Surveys were conduct- The extent to which butterflies and birds affect ed between 0900 and 1130 h on days with con- outcrossing was assessed by counting flowers visited stant sunlight between 2 November and 15 De- by pollinators during single foraging bouts at trees cember 1997, during the peak flowering period of from the moment of arrival to departure to another D. obtusifolius. tree. I assumed a correlation between the number of sequentially visited flowers and the proportion TREE DENSITY, SIZE AND FLOWER AND FRUIT PRODUC- of flowers that are self-pollinated through pollen TION. At each forest area (U, M, and D), the carryover. Observations on flower visits by butterfly number and DBH of D. obtusifolius trees exceeding pollinators descombesi, Atrophaneura adam- 10 cm were recorded in three 1 ha plots. The plots soni, and Troides aecus, and also by sunbirds and were separated by at least 1 km. The internodes of leafbirds, were made at two trees in the undis- the main axis of D. obtusifolius panicles are clearly turbed site selected for their similar size and com- developed, allowing buds and flowers produced on parable distances to nearest neighbors. each panicle to be counted even after flower ab- Flower visitation by nocturnally active sphingid scission. Fruit production could therefore be as- moths could not be recorded directly but was in- sessed as a proportion of flowers produced. At peak ferred by catching moths at light traps and iden- flowering during November 1997, flowers, buds, tifying pollen types collected from the tongue and and abscised flowers were counted using a 25–56x head. A 2 m2 white sheet was suspended vertically Nikon telescope on a random sample of 30 panicles 50 cm–2.5 m above ground. We attached a 1.5 m on 30 trees at U, M, and D. Fruit production was long 65W white fluorescent bulb powered by a counted in February 1998, when developing fruit Indirect Effects on Pollination 159

TABLE 1. Cover of herbaceous flower-bearing at undisturbed (U), moderately disturbed (M), and disturbed (D) sites at Huay Kha Khaeng. Ground cover of the invasive Chromolaena odorata is singled out as this species contributed greatly to site differences. Kruskal–Wallis test was applied to untransformed data.

No. species Species per plot Ground Cover (%) C. odorata (% cover) Site total x¯ Ϯ SE (median) x¯ Ϯ SE (median) x¯ Ϯ SE (median) U 14 3.8 Ϯ 0.2 (3.7) 12.3 Ϯ 0.6 (12.3) 0.08 Ϯ 0.08 (0) M 17 2.8 Ϯ 0.3 (3.0) 12.3 Ϯ 1.8 (10.3) 0.33 Ϯ 0.26 (0) D 10 3.0 Ϯ 0.2 (3.0) 42.4 Ϯ 4.8 (43.5) 30.8 Ϯ 2.8 (30) H(2) 12.007 25.657 161.5 P 0.0025 Ͻ0.001 Ͻ0.001 could be clearly distinguished but had not yet at- cent and was consistently higher than the other two tained full size. Fruit production was determined forest regions. This difference in cover was largely for a random sample of at least 40 panicles on 30 due to the exotic invader C. odorata (Asteraceae), trees from each of the three forest locations. Fruit which dominated many disturbed site plots (66% production can be directly equated with seed pro- of herbaceous cover) but occurred only occasionally duction because dipterocarp fruit contain only a at M (2.9% of herbaceous cover) and U (0.4% of single seed. herbaceous cover; Table 1). Pavonia sp. () was likewise widespread at D, occurring in 17 of STATISTICAL ANALYSIS. The labels D, M, and U de- 20 transects compared to only 8 at M and 5 at U. scribe the set of research plots located within single At U, only Desmodium amethystinum (Papilionoi- S blocks of forest that, although large, are continuous deae) achieved a ground cover value exceeding 5 PECIAL and not randomly distributed across the landscape. percent and even then only in a single plot. In To maximize data independence, observation trees contrast, eight species at M and five at D exceeded and butterfly transects were widely spaced within 5 percent cover in at least one plot. the three forest blocks. While treatment effects can- S ECTION not be separated strictly from site effects, a Mantel POLLINATOR ACTIVITY. Three pierid and two pa- test across all transects at the three sites failed to pilionid butterflies were observed regularly at flow- find a relationship between geographic proximity ers of D. obtusifolius. Pollinator activity was dom- and similarity in butterfly composition, suggesting inated by Delias descombesi and D. acalis (), that the transects were spaced sufficiently apart to which were present at all locations, although their be considered statistically independent (Ghazoul flower visitation frequency was highest at trees at 2002a). The trees used in this study were even U and lowest at D (Table 2). Atrophaneura adam- more widely spaced than the transects and were soni (Papilionidae) was frequently observed visiting therefore treated as true replicates of the three dis- flowers at U and M but was rarely seen to do so turbance treatments. at D. Catopsilia pomona (Pieridae) and T. aecus (Pa- When necessary, data were arcsine or log trans- pilionidae) visited flowers infrequently at all sites. formed as appropriate to obtain normality. Analysis Sunbirds Nectarinia spp. and leafbirds Chlorop- of variance or nested ANOVA was applied to nor- sis spp. regularly visited D. obtusifolius flowers at D malized data; otherwise, if normality was not only. Pollen was carried on the lores and bases of achieved after transformation, the nonparametric bills, and contact with the stigma was observed on Kruskal–Wallis or Mann–Whitney test was applied every flower visit. At D, sunbirds accounted for 52 to untransformed data. Analyses were performed percent of pollinator activity, and leafbirds 16 per- with STATISTICA (StatSoft Ltd.). cent (Table 2). Leafbirds were seen pollinating D. obtusifolius flowers at M (but not during periods of RESULTS data collection) and the apparent lack of leafbird pollinator activity in moderately disturbed forest TREE DENSITY AND SITE VEGETATION CHARACTERIS- (Table 2) is thus misleading. Compared to butter- TICS. A total of 29 flower-bearing herbaceous spe- flies, birds were of minor importance as flower vis- cies was recorded. Percent cover increased and spe- itors at U, where their combined pollination activ- cies richness decreased with increasing disturbance ity accounted for less than 3 percent of all diurnal severity (Table 1). Percent ground cover of herba- visits. Thus, the pronounced decline in pollination ceous plants at D ranged between 20 and 60 per- by butterflies at D was offset to some extent by an 160 Ghazoul a b c ? 0.001 0.004 (0) Ϫ 0.03 (0.12) 0.06 (0.28) SE (median). 39.13 Ͻ Ϯ Ϯ Ϯ

Ϯ p A. adamsoni ¯ 0.33 0.17 0.004 ups to disturbance are a b c spp. 0.001 Ϫ 0.02 (0) 0.08 (0.42) 0.07 (0.14) 40.03 Ͻ Ϯ Ϯ Ϯ p . Delias 0.23 0.03 0.53 FIGURE 1. Number of flowers visited by pollinators during a visit to a single Dipterocarpus obtusifolius tree. Birds, particularly the sunbirds, and the large birdwing butterfly Troides aecus visited significantly fewer flowers on each single visit to a tree than the butterflies Delias 0.012 (0) 0.02 (0) ϭ at U, M and D. All values presented as x NS descombesi and Atrophaneura adamsoni. Sample sizes are (385) — (0) Ϯ Ϯ given within the bars. 0.05 0.024 increase in bird activity, but not sufficiently to ’ if there was no significant change avoid a significant decline in diurnal pollinator ac- ϭ tivity on D. obtusifolius at D (Table 2) relative to 0.002 (0) 0.04 (0.08) U and M. ϩ 0.001 ECTION Ϯ (137) Ϯ — (0) Diurnal pollinator species differed significantly Ͻ Dipterocarpus obtusifolius S in the number of flowers visited in each tree (Fig. 0.16 0.002 1; mixed model two-way ANOVA: F4, 113 ϭ 4.84, P ϭ 0.001; no significant difference among data a a b from the two trees). On average, a greater number

PECIAL of flowers were visited within a tree by Delias spp. S

’ if abundance declined, and ‘ and A. adamsoni than by T. aecus, sunbirds, or leaf-

Ϫ

Ϫ birds. 0.001 0.11 (0.52) 0.16 (0.43) 0.03 (0.07) 30.1 Ͻ Catches of sphingid moths were low (Table 3), Ϯ Ϯ Ϯ ranging from 3 to 18 per trap night across all sites. 0.86 0.70 0.10 There was no significant difference in the number of sphingids across sites (Table 3). Between 25 and a a b 30 percent of moths were found to be carrying Dipterocarpus pollen, and there was no significant difference among sites in this respect (Table 3). Ϫ 0.001 0.10 (0.77) 0.16 (0.43) 0.07 (0.19) 40.55 Ͻ Ϯ Ϯ Ϯ TABLE 3. Abundance of sphingid moths (numbers per 0.70 0.89 0.31 trap per night), and proportion bearing Dip- terocarpus obtusifolius pollen, at light traps during three-hour observation periods at 12 lo- ’ if abundance increased with disturbance, ‘ 37 29 22 cations at U, M and D. Results are x¯ Ϯ SE. ϩ

Moths bearing D. obtusifolius Site Sphingid abundance pollen (%) Activity as visits per minute of butterfly and bird pollinators in the crowns of Kruskal–Wallis (H-statistic) or Mann–Whitney (U statistic) non-parametric tests were applied to data as appropriate. Responses of pollinator gro illustrated by ‘ U 9.4 Ϯ 0.6 26 M 8.9 Ϯ 1.0 30 Site No. Trees All flower-visitors ButterfliesD Sunbirds11.0 Ϯ Leafbirds 1.1 26 or (U-statistic) F(2, 33) ϭ 1.07

(2) P NS TABLE 2. U M D Response H P Indirect Effects on Pollination 161

TABLE 4. Abundance of butterfly pollinators along 20 transects at U, M and D (numbers per transect). Medians in bold with lower and upper quartiles in brackets. Analysis of variance (F) was conducted on square root transformed data for total pollinator abundance, the results of which are presented as x¯ Ϯ SE. Kruskal–Wallis (H) tests were applied to all other categories as these remained non-normal even after transformation. Responses of butterfly families to disturbance are illustrated by ‘ϩ’ if abundance increased with disturbance, ‘Ϫ’ if abundance declined, and ‘ϭ’ if there was no significant change.

All butterfly Site D. descombesi C. pomona A. adamsoni T. aecus pollinators U 2 (0, 3.5) 1 (1, 3.5) 0 (0, 1) 0 (0, 0) 3.6 Ϯ 0.6 M 1.5 (0, 3) 2.5 (0, 3.5) 1 (1, 3) 0 (0, 0) 4.0 Ϯ 0.6 D 1 (0, 1) 2.5 (0.5, 5.5) 1 (0, 3) 1 (0, 1) 4.0 Ϯ 0.6 Direction Ϫ ϭ ϩ ϩ ϭ H(2) or (F2, 57) 5.64 0.61 7.36 16.83 (0.27) P 0.060 NS 0.025 Ͻ0.001 NS

BUTTERFLY POLLINATOR SPECIES ABUNDANCE. Over- 1), presumably in response to increased light pen- all abundance of butterfly pollinators did not differ etration in the more open disturbed (Ka- significantly among the three sites (Table 4), al- bakoff & Chazdon 1996, Ostertag 1998). The in- though this result masks differences at the species crease in understory flowering plant cover implies level. Abundance of A. adamsoni and T. aecus in- increased availability of understory floral nectar re- creased at D and M relative to U, while D. descom- sources at D. In particular, the invasive exotic C. S

besi decreased. No difference in the abundance of odorata, the most widespread herbaceous plant at PECIAL the occasional pollinator C. pomona was recorded, disturbed sites, presented large numbers of flowers and other occasional pollinators were observed too that were frequently visited by butterflies. In con- infrequently for meaningful statistical analysis. trast, canopy floral resources were similar across the

three sites, as D. obtusifolius was the only common S

TREE DENSITY, SIZE, AND FLOWER AND FRUIT PRODUC- flowering tree during the study period and no dif- ECTION TION. Density of D. obtusifolius within the nine ferences in its density, size, or flower production plots ranged from 24 to 41 trees/ha but there was (Table 5) across sites were recorded. no significant difference in density or tree size This shift in the relative abundance of floral across sites (Table 5). Flower production between resources from the canopy to the understory at dis- sites and among trees within a site was similar (Ta- turbed locations attracted butterfly pollinators of ble 5; nested ANOVA on between site variance: F2 D. obtusifolius to the understory, resulting in low ϭ 0.60, N.S.). Fruit production was also similar diurnal pollinator activity on D. obtusifolius (Table across trees and there was no discernible site effect 2). Indeed, an earlier study showed that D. obtu- (Table 5). sifolius flowers at D that were visited by pollinators were more likely to receive incompatible cross-spe- DISCUSSION cies pollen, indicating that these pollinators were visiting other pollen sources in the understory At Huay Kha Khaeng, extraction of S. siamensis (these being the only alternative available) more over recent decades has resulted in a marked in- frequently (Ghazoul 2002b). Additionally, the crease in understory flowering plant cover (Table overall decrease in abundance of other (non-cano-

TABLE 5. Density, size (diameter at breast height), and flower and fruit production of Dipterocarpus obtusifolius trees at U, M and D. Density and size data derived from three 1 ha plots at each site.

D. obtusifolius D. obtusifolius size Flowers per panicle Fruit per panicle Site density (N/ha) DBH (cm Ϯ SE) (x¯ Ϯ SE) (x¯ Ϯ SE) U 33.3 Ϯ 4.1 31.7 Ϯ 1.8 4.06 Ϯ 0.07 1.06 Ϯ 0.03 M 30.0 Ϯ 3.1 32.9 Ϯ 1.4 4.16 Ϯ 0.06 1.08 Ϯ 0.04 D 29.0 Ϯ 2.6 28.3 Ϯ 1.0 4.11 Ϯ 0.06 1.12 Ϯ 0.04 F(2, 6) ϭ 0.47 F(2, 27) ϭ 1.52 F(2, 27) ϭ 0.79 F(2, 27) ϭ 1.49 NS NS NS NS 162 Ghazoul

py) butterfly species at disturbed sites (Ghazoul early stage of development. In this respect, Delias 2002a) may result in reduced demand on nectar in spp. and A. adamsoni are likely to cause more self- the understory, thus further increasing the avail- pollinations because they visit more flowers within ability of nectar in the understory relative to the a single canopy before moving to neighboring trees canopy. (Fig. 1) and are consequently less likely to be ef- Differences in pollinator activity across sites fective pollinators. The large butterfly T. aecus, to- cannot be explained by the overall abundance of gether with sunbirds and leafbirds, visited fewer D. obtusifolius pollinators because this did not flowers within each canopy (Fig. 1) and are there- change across sites (Table 4). Some canopy spe- fore expected to promote outcrossing by virtue of cialists, such as Delias spp., did indeed decline at more inter-tree movements relative to the total disturbed sites (D and M), but this was offset by number of flowers visited (as well as increased po- an increase in other pollinators such as the papilio- tential for pollen carryover), given that they have nid A. adamsoni (Table 4). At disturbed sites, how- larger pollen loads that can be carried to greater ever, A. adamsoni was only observed in the under- numbers of flowers. Declining flower visits by but- story, whereas at U it almost exclusively occurred terflies may therefore be offset by a moderate in- in the canopy (Ghazoul, pers. obs.). Shifts in the crease in pollination by birds. vertical distribution of butterflies in open forest ar- Pollination by multiple taxa buffers plants from eas have been noted before (Spitzer et al. 1993, disturbances that affect the behavior of one of the Beccaloni 1997, Spitzer et al. 1997, DeVries et al. taxa—in this case, butterflies. Despite reduced but- 1999), although without specific reference to nec- terfly visitation to trees in the most intensively tar resource distribution. The high activity of sun- logged areas, no effect on reproductive output was birds in D. obtusifolius canopies in the disturbed observed because of partial compensation by birds areas likely reflects their preference for open areas and, presumably, moths. Plants that lack options (Lambert 1992, Thiollay 1995). for compensatory pollination are more susceptible Dipterocarpus obtusifolius is also pollinated by to reduced fruit set following a decline or loss of ECTION endothermic sphingid moths (Ghazoul 1997) that their principal pollinators (Johnson 1992, Rathcke S require plentiful nectar to maintain high energy ex- 2000). Thus, S. siamensis, which lacks such diver- penditure (Casey 1976). Small herbaceous flowers sity of pollinators, exhibited marked reduction of produce little nectar that is generally unavailable at reproductive output across the sites as a result of night and are therefore unlikely to attract moths changes in the foraging behavior of its Trigona bee PECIAL from the canopy. Light trap results indicated no pollinators (Ghazoul et al. 1998). S differences in sphingid moth abundances across Recent studies have highlighted the negative sites or in the proportion of sphingids carrying D. implications of disturbance on pollinator diversity obtusifolius pollen. Therefore, observed differences and abundance for plant reproductive success and in the efficacy of pollination across sites were most the structure of plant communities (Bond 1994, likely attributable to diurnal pollinators. Parra-Tabla et al. 2000, Rathcke 2000). This study Despite relatively few flower visits at disturbed and others (Ghazoul et al. 1998, Cunningham site trees, fruit production at this site was not sig- 2000) demonstrate that disturbance can also dis- nificantly different than at U and M. This suggests rupt pollination processes by causing changes to resource-limited fruit set in D. obtusifolius rather the foraging behavior of pollinators rather than to than limitation by insufficient pollination. In a pre- their abundance. This conclusion has relevance be- vious study, however, 68 percent of artificially yond the circumstances of this study, and particu- cross-pollinated flowers developed into mature fruit larly where invasive species have caused ecological compared to only 25 percent of open-pollinated change (Gigord et al. 1999). For example, the West flowers (Ghazoul 1997), indicating both abundant Indian herbaceous plant Lantana camara is now resources for fruit development and possible pollen widely established across tropical zones and has be- limitation (cf. Dudash & Fenster 1997 on deter- come the dominant understory herb in many mining pollen and resource limitation). Inverte- southern Asian forests. Because this butterfly- and brate seed predation, which can cause early fruit bird-pollinated plant occurs at very high densities abortion, is not important because it affects less and produces flowers and fruits throughout the than 10 percent of fruit and shows no pattern year, it could potentially cause a shift in the distri- among sites (Ghazoul 1997). Dipterocarpus obtusi- bution of forest floral resources and consequently folius is self-incompatible and a large proportion of affect the foraging behavior of native pollinators. fruit derived from selfed flowers are aborted at an This may account for the declining reproductive Indirect Effects on Pollination 163 output of some native trees in these forests (Murali maintenance of biodiversity in managed natural et al. 1996). forests (Didham et al. 1996, Ghazoul and Hellier A further implication of this study is that mon- 2001), and management strategies designed to con- itoring the abundance of species that contribute to serve ecological processes are easier to devise and mutualistic interactions may not be sufficient to have greater chance of success than strategies that determine the state of those interactions. Rather, aim to conserve biodiversity directly (Lugo 1995). monitoring changes in the processes mediated by those interactions may improve predictions of fu- ACKNOWLEDGMENTS ture community composition over those that ex- trapolate from recent trends in local abundance. I am grateful for support from Mr. C. Pitdamkhan and Ecological processes, as the sum of multispecies in- the staff of Huay Kha Khaeng Wildlife Sanctuary, Dr. C. teractions, are more representative of forest resil- Hutacharern and K.Chaisurisri of the Royal Forest De- ience and less sensitive to natural variability than partment, and J. Coles at the ASEAN Forest Tree Seed Centre. Field research was conducted with the assistance numerical assessments of species richness or pop- of N. Pornsurat, K. Liston, and A. Macgregor. Permission ulation abundance. Indeed, process-orientated to conduct research in Thailand was granted by the Na- measures are currently preferred for assessing the tional Research Council of Thailand.

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