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

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Alien Abduction: Disruption of Native Plant-Pollinator Interactions by Invasive Species1 BIOTROPICA 36(2): 156±164 2004 Alien Abduction: Disruption of Native Plant-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 butter¯y-, 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 ¯owering plant cover, dominated by the exotic invader Chromolaena odorata. Activity of butter¯y 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 suf®cient 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 butter¯y pollinators rather than their abundance. A shift in the relative abundance of ¯oral 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 butter¯ies, 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 butter¯y pollination. ECTION S Key words: compensation; Dipterocarpaceae; disturbance; invasive species; 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 animal-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 ¯oral 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 ¯oral resources by inef®cient 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 habitat 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, ®delity pollinating insects. 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 ¯oral resources in the forest landscape, of ¯oral 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: 1(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 6 10/ha (xÅ 6 SE, N 5 20). lius, a common sympatric dipterocarp tree. The Observations were made through the entire extent speci®c 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 6 8/ha (xÅ 6 SE, N SPECIES AND STUDY SITES. Dry deciduous forests 5 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 ef®cient system of ®re 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 ®re occurred ®ve years be- S Sanctuary, Uthai Thani Province, western Thailand fore the start of the work and this had affected all ECTION (158369N, 998209E). 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 ®nd 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 ¯owers annually from Oc- cades has created a gradient of decreasing distur- tober to January. The self-incompatible ¯owers 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 butter¯ies, 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 lea¯ess 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 (.10 cm diameter at breast between 15 to 25 m, allowed for easy observation height [DBH]) density in this area averaged 117 6 of ¯ower and fruit production and pollinator ac- 8/ha (xÅ 6 SE, N 5 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 ¯owering 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 butter¯y census transect small numbers (full details given in Ghazoul et al. (described below). Each ¯ower-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 ¯owering plant cover in each plot. It was butter¯y transects (see below) in the three forest not possible to identify all species, but each was regions.
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