BlOTROPlCA 36(2): 156-1 64 2004

Alien Abduction: Disruption of Native Plant-Pollinator Interactions

by lnvasive Species’

Jaboury Ghazou12
Department of EnvironmentalScience 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 . obtusifoiius 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 Chromokzena odorata. Activity of butterfly pollinators at D . obtusifoiius 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. obtusifoliw, 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
Z invasion by C. odorata, led to a parallel shift in foraging location of the principal diurnal pollinators, the butterflies,
0 toward the understory. Despite reduced pollination at disturbed sites, behavioral changes did not translate into a D.
F obtusifoiius seed set effect, possibly because pollination by birds (or moths) at the disturbed site compensated for
Y
cn
reduced butterfly pollination.

Kg worh: compensation; Dipterocatpaceae; disturbance; invasive species; pollination; reproductive success, seed set; tropical
J d y firest
5
Y
a TROPICAL TREES ARE MOSTLY SELF-INCOMPATIBLE and caused by disturbance may lead to the restructuring
cn 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 e t a/.
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 lkgonu 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, fidelity 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 hnction 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-
1 Received 30 October 2003; revision accepted 12 Feb-
linators in that landscape (Chittka & Schurkens
ruary 2004. 2001). In this study, I investigated how extraction
E-mail: j.ghazoul@imperial.ac.uk; Fax: +(0)20 7594 of S. siamensis results in changes in habitat struc-
2308. ture and composition, particularly in terms of in-

156

vasion of the forest understory by an alien plant
Cbromokzena odorata, and how this in turn affects
the reproductive ecology of Dipterocarpus obtusifo-
olius, a common sympatric dipterocarp tree. The
specific aims of this study were to compare (1) un-
derstory plant composition, (2) abundance of lep-
idopteran pollinators of D. obtusi~%fius,(3) polli-
nator activity at D. obtusifoolius trees, and (4) repro-
ductive output of D. obtusifofius across three sites
differing in intensity of S. siarnensis extraction.
METHODS
SPECIES AND STUDY SITES.-DV deciduous forests
(DDF) in Thailand are dominated by four tree spe-
cies belonging to two genera, Shorea and Diptero-
carpus (Dipterocarpaceae). Prior to a national log-
ging ban in 1989, s. siarnensis Miq. and s. obtusa
Wall. ex B1. were extracted commercially from
many forests, leaving D. tubercukztus Roxb. and D .
obtuszj5olius Teijsm. intact. Since then, illegal small-
scale extraction of Shorea (mostly for domestic use)
has continued. The resulting degraded forests have
reduced densities of Shorea but not Dipterocarpus.
This study, conducted from October 1997 to
April 1998, used DDF areas of differing distur-
bance intensity at Huay Kha Khaeng Wildlife
Sanctuary, Uthai Thani Province, western Thailand
(15”36‘N, 99’20’E). Huay Kha Khaeng (HKK)
has a total area of 2575 km2; 381 km2 is DDF,
most of which occurs in a single 260 km2 block
on the eastern edge of the sanctuary (Nakhasathien
& Stewart-Cox 1990) where this work was con-
ducted. Anthropogenic disturbance over two de-
cades has created a gradient of decreasing distur-
bance intensity from the edge of the sanctuary to
its interior. Three areas were selected to represent
this gradient.
Three undisturbed sites (labeled collectively as
U) were located in a 3 x 6 km area within the
much larger “undisturbed forest region where hu-
man interference is strictly prohibited and ade-
quately enforced. Tree ( > l o cm diameter at breast
height [DBH]) density in this area averaged 117 2
8/ha (22 SE, N = 20; Ghazoul et af. 1998). Un-
disturbed forest extended from ca 9 krn within the
sanctuary boundary to its interior and research
plots were located in a region 14-20 km within
the sanctuary boundary.
In moderately disturbed forest areas (M), and
prior to the relocation of villages outside the sanc-
tuary in 1990, Shorea trees had been extracted in
small numbers (full details given in Ghazoul et al.
1998). Since then this region, located 3-9 km
Indirect Effects on Pollination 157
within the park boundary, has been subject to the
same strict controls as the undisturbed sites. Tree
densities averaged 101 2 lO/ha ( f ? SE, N = 20).
Observations were made through the entire extent
of moderately disturbed forest, which covered an
area of ca 15 km2.
Highly disturbed forest exists in a 3-5 km wide
buffer zone that extends along the length of the
northeastern boundary of the sanctuary for ca 15
krn. Prior to the designation of the buffer zone in
1990, this area was subject to widespread extrac-
tion of S. siarnensis that resulted in the currently
low total tree densities of 73 2 8/ha (2 t SE, N
= 20). Disturbed (D) study sites were within a 10
km2 area within this buffer zone.
All sites were located within the same forest
basin and had similar elevations and topography.
The soil is homogeneous throughout the basin,
with no apparent major differences between sites
in soil depth, pH, organic content, or water, nitro-
gen, potassium, and phosphorous availability (Gha-
zoul, pers. obs.). Grazing and small-wood collec-
v)
tion are prohibited in the sanctuary but limited 73
grazing by cattle is permitted in the buffer zone. m
An efficient system of fire control and prevention 0
had been established by park authorities, such that
the most recent major fire occurred five years be-
v)
fore the start of the work and this had affected all m
three study areas. Indeed, selection of areas for
study was constrained by the need to find areas
9
with similar disturbance histories other than log-
5
ging.
At Huay Kha Khaeng, D. obtus$ilius produces
its large funnel-shaped flowers annually from Oc-
tober to January. The self-incompatible flowers are
produced alternately on panicles and are pollinated
by butterflies, moths, and, occasionally, birds (Gha-
zoul 1997). In common with many other trees in
this forest type, D. obtusifofius is deciduous and is
leafless from November to late January or early
February. The deciduous nature of this tree and the
forest generally, together with its modest height of
between 15 to 25 m, allowed for easy observation
of flower and fruit production and pollinator ac-
tivity.
SITE VEGETATION CHARACTERISTICS-TO estimate
changes in the composition of the forest understory
following removal of S. siarnensis trees, understory
flowering plant cover and species richness were re-
corded in 6 m radius plots (113 m2) at the start,
middle, and end of each butterfly census transect
(described below). Each flower-bearing plant spe-
cies was given a percent cover estimate by taking
 158 Ghazoul
the mean of independent estimates made by two
observers. Summing percent cover across all species
gave total flowering plant cover in each plot. It was
not possible to identify all species, but each was
allocated a unique code and samples were taken to
confirm identities at other locations.
POLLINATOR AcnwrY.-The large pendant D. ob-
tusifolius flowers are pollinated by moths, butter-
flies, and birds. Anthesis occurs at ca 2000 h and
stigmatic surfaces remain receptive, and pollen vi-
able, to noon on the following day (Ghazoul
1997). Nectar secretion begins about one hour af-
ter anthesis and continues to early afternoon on the
following day. Full details of the pollination biol-
ogy of D. obtusifolius are found in Ghazoul (1997).
Using binoculars (Leica 8 x 32 and 10 x 42) and
a field telescope (Nikon 25-5Gx magnification), the
activities of butterfly and bird pollinators were re-
corded by noting their abundance in D. obtusifolius
canopies at each of the three study sites. The num-
z ber and species identity of flower visitors in D. ob-
0 tusifolius crowns were recorded during one-minute
F observation periods at ten-minute intervals. Obser-
0 vations at each tree were continued for three hours
W
cn between 0830 and 1200 h, overlapping the period
of stigma receptivity, and for 30 trees at each site.
1
5 To maximize independence of data, distances be-
Ya tween neighboring observation trees were at least
220 m. Each tree was used only once. Observations
cn were undertaken from 21 October 1997 to G Jan-
uary 1998, coinciding with the peak D. obtusi$lius
flowering season. Weather conditions remained dry
and sunny throughout this period.
The extent to which butterflies and birds affect
outcrossing was assessed by counting flowers visited
by pollinators during single foraging bouts at trees
from the moment of arrival to departure to another
tree. I assumed a correlation between the number
of sequentially visited flowers and the proportion
of flowers that are self-pollinated through pollen
carryover. Observations on flower visits by butterfly
pollinators Delia descombesi, Atrophaneura adam-
soni, and Troides aecus, and also by sunbirds and
leabirds, were made at two trees in the undis-
turbed site selected for their similar size and com-
parable distances to nearest neighbors.
Flower visitation by nocturnally active sphingid
moths could not be recorded directly but was in-
ferred by catching moths at light traps and iden-
tifying pollen types collected from the tongue and
head. A 2 m2 white sheet was suspended vertically
50 cm-2.5 m above ground. We attached a 1.5 m
long 65W white fluorescent bulb powered by a
12V car battery to the top edge of the sheet. Light
trapping was conducted at the center of each of 12
butterfly transects (see below) in the three forest
regions. Two sets of light-trapping equipment per-
mitted two transects to be sampled simultaneously,
and these were selected randomly from the total set
until 12 transects per site had been completed.
Light trapping was only carried out on relatively
dark nights ( i e . , from waning to waxing half-
moons) and from 2100 to 2400 h continuously.
Sphingid moths attracted to the light were caught
with a hand net and transferred to transparent plas-
tic boxes lined with tissue paper to which some
drops of ethyl-acetate had been applied. Dead
moths were transferred into paper envelopes and
labeled. Tissue paper was replaced and fresh ethyl-
acetate was applied after each capture. The pro-
portion of moths carrying D. obtusifolius pollen was
determined using a binocular microscope.
BUITERFLY POLLINATOR ABUNDANcE.-Butterfly pol-
linators of D. obtus$liur were surveyed for 30 min-
utes along each of 20 transects (500 m) at each
site. Each transect was surveyed only once. Tran-
sects were located as far as possible from existing
tracks and paths. Within a site, transects were
mostly parallel to each other and adjacent transects
were separated by at least 200 m and up to ca GOO
m. Two observers recorded butterflies within an es-
timated 20 m each side of the transect. Binoculars
aided identification and care was taken to avoid
counting the same butterfly twice. Species were
identified using Pinratana (1979, 1983, 1988) and
Pinratana and Eliot (1992). Surveys were conduct-
ed between 0900 and 1130 h on days with con-
stant sunlight between 2 November and 15 De-
cember 1997, during the peak flowering period of
D. obtusifilius.
TREEDENSITY, SIZE AND FLOWER AND FRUIT PRODUC-
TIoN.-At each forest area (U,M, and D), the
number and DBH of D. obtusz$lius trees exceeding
10 cm were recorded in three 1 ha plots. The plots
were separated by at least 1 km.The internodes of
the main axis of D. obtusi$lius panicles are clearly
developed, allowing buds and flowers produced on
each panicle to be counted even after flower ab-
scission. Fruit production could therefore be as-
sessed as a proportion of flowers produced. At peak
flowering during November 1997, flowers, buds,
and abscised flowers were counted using a 25-56x
Nikon telescope on a random sample of 30 panicles
on 30 trees at U, M, and D. Fruit production was
counted in February 1998, when developing fruit

TABLE 1. Cover of herbaceous fiower-bearing plants at undisturbed (U), moderately disturbed (M), and disturbed (0)
sites at Huay Kha Khaeng. Ground couer of the inuasiue Chromolaena odorata is singled out LLT this species
contributed greatly to site differences. Kruskal- Wallis test was applied to untransformed data.
No. species Species per plot
Site toral f t SE (median)
U 14 3.8 t 0.2 (3.7)
M 17 2.8 5 0.3 (3.0)
D 10 3.0 2 0.2 (3.0)
12.007
0.0025
could be clearly distinguished but had not yet at-
tained full size. Fruit production was determined
for a random sample of at least 40 panicles on 30
trees from each of the three forest locations. Fruit
production can be directly equated with seed pro-
duction because dipterocarp fruit contain only a
single seed.
STATISTICAL ANALYsis.-The labels D, M, and U de-
scribe the set of research plots located within single
blocks of forest that, although large, are continuous
and not randomly distributed across the landscape.
To maximize data independence, observation trees
and butterfly transects were widely spaced within
the three forest blocks. While treatment effects can-
not be separated strictly from site effects, a Mantel
test across all transects at the three sites failed to
find a relationship between geographic proximity
and similarity in butterfly composition, suggesting
that the transects were spaced sufficiently apart to
be considered statistically independent (Ghazoul
2002a). The trees used in this study were even
more widely spaced than the transects and were
therefore treated as true replicates of the three dis-
turbance treatments.
When necessary, data were arcsine or log trans-
formed as appropriate to obtain normality. Analysis
of variance or nested ANOVA was applied to nor-
malized data; otherwise, if normality was not
achieved after transformation, the nonparametric
Kruskal-Wallis or Mann-Whitney test was applied
to untransformed data. Analyses were performed
with STATISTICA (Statsoft Ltd.).
RESULTS
TREEDENSITY AND SITE VEGETATION CHARACTERIS-
TICS.-A total of 29 flower-bearing herbaceous spe-
cies was recorded. Percent cover increased and spe-
cies richness decreased with increasing disturbance
severity (Table 1). Percent ground cover of herba-
ceous plants at D ranged between 20 and 60 per-
Indirect Effects on Pollination 159
Ground Cover (Yo) C. odorata (% cover)
f ? SE (median) f 2 SE (median)
12.3 t 0.6 (12.3) 0.08 i. 0.08 (0)
12.3 i. 1.8 (10.3) 0.33 5 0.26 ( 0 )
42.4 ? 4.8 (43.5) 30.8 2 2.8 (30)
25.657 161.5
<0.001 <O.OOl
cent and was consistently higher than the other two
forest regions. This difference in cover was largely
due to the exotic invader C odorata (Asteraceae),
which dominated many disturbed site plots (66%
of herbaceous cover) but occurred only occasionally
at M (2.9% of herbaceous cover) and U (0.4% of
herbaceous cover; Table 1). Pavonia sp. (Malvaceae)
was likewise widespread at D, occurring in 17 of
20 transects compared to only 8 at M and 5 at U.
At U, only Desmodium arnethystinum (Papilionoi-
deae) achieved a ground cover value exceeding 5
percent and even then only in a single plot. In
contrast, eight species at M and five at D exceeded
5 percent cover in at least one plot.
POLLINATOR AcTivlTu.-Three pierid and two pa-
pilionid butterflies were observed regularly at flow-
ers of D. obtwif0liu.r. Pollinator activity was dom-
inated by Delim &scombesi and D. acalis (Pieridae),
which were present at all locations, although their
flower visitation frequency was highest at trees at
U and lowest at D (Table 2). Atrophaneura adam-
soni (Papilionidae) was frequently observed visiting
flowers at U and M but was rarely seen to do so
at D. Catopsiliapomona (Pieridae) and I: aecw (Pa-
pilionidae) visited flowers infrequently at all sites.
Sunbirds Nectarinia spp. and leafbirds Chlorop-
sis spp. regularly visited D. obtwifoliusflowers at D
only. Pollen was carried on the lores and bases of
bills, and contact with the stigma was observed on
every flower visit. At D, sunbirds accounted for 52
percent of pollinator activity, and leafbirds 16 per-
cent (Table 2). Leafbirds were seen pollinating D.
obtwzjdius flowers at M (but not during periods of
data collection) and the apparent lack of leafbird
pollinator activity in moderately disturbed forest
(Table 2) is thus misleading. Compared to butter-
flies, birds were of minor importance as flower vis-
itors at U, where their combined pollination activ-
ity accounted for less than 3 percent of all diurnal
visits. Thus, the pronounced decline in pollination
by butterflies at D was offset to some extent by an
 160 Ghazoul

0
-
Median
Outliers

T
0

Deltas Afmphaneura Tmides Sunbirds Lealbirds

descombesr sdamsonr aecus

FIGURE 1 . Number of flowers visited by pollinators

h
during a visit to a single Dipterocarpw obtusifolius tree.
O h Birds, particularly the sunbirds, and the large birdwing
- 0v
butterfly Troidps aecw visited significantly fewer flowers
2-m
gsg II gz on each single visit to a tree than the butterflies Delia
+I I tl - desrombesi and Atrophaneura ahmoni. Sample sizes are
given within the bars.

increase in bird activity, but not sufficiently to

avoid a significant decline in diurnal pollinator ac-
tivity on D. obttlsifolius at D (Table 2) relative to
U and M.
W Diurnal pollinator species differed significantly
cn in the number of flowers visited in each tree (Fig.
-I
1; mixed model two-way ANOVA: F4,113 = 4.84,
9 P = 0.001; no significant difference among data
Ya from the two trees). O n average, a greater number
of flowers were visited within a tree by D e l i a spp.
cn and A. adamsoni than by T aecw, sunbirds, or leaf-
birds.
+I +I t I Catches of sphingid moths were low (Table 3),
w o z
W b
ranging from 3 to 18 per trap night across all sites.
000 There was no significant difference in the number
of sphingids across sites (Table 3). Between 25 and
30 percent of moths were found to be carrying
Dipterocarpus pollen, and there was no significant
difference among sites in this respect (Table 3).
+I +I t l
no%-
=??Z TABLE 3. Abundznce of sphingid moths (numbers per
trap per night), and proportion bearing Dip-
terocarpus obtusifolius polkn, at light traps
h m N during three-hour observation periods at 12 ln-
rn" cations at U, M and D. Results are f SE. _f

Moths bearing
h D. obtusifoliuc
.- Site Sohingid abundance Dollen (%)
.-
YI

n
Y U 9.4 5 0.6 26
M 8.9 ? 1.0 30
D 11.0 ? 1.1 26
F(2, 33) = 1.07
P NS
 Indirect Effects on Pollination 161

TABLE 4. Abundance of butterflv pollinators along 20 transects at U, M and D (numbers per transect). Medians in bola'
with lower and upper quartiles in brackets. Analyss of variance (F) was conducted on square root transformed
data for total pollinator abundance, the results of which are presented ar f 2 SE. Krwkal- Wallis (H) tests
were applied to all other categories as these remained non-normal euen ajer transformation. Responses ofbutte$y
families to disturbance are illustrated by '+ ' ifabundance increased with disturbance, '- 'ifabundance declined,
if
and '= ' there was no signifcant change.

All butterfly
Site D. descombesi C. pomona A. d m s o n i 7: aecus pollinators
U 2 (0,3.5) 1 (1, 3.5) 0 (0, 1 ) 0 (0,0) 3.6 5 0.6
M 1.5 (0, 3) 2.5 (0,3.5) 1 (1, 3) 0 (0,0) 4.0 ? 0.6
D 1 (0,1 ) 2.5 (0.5, 5.5) 1 (0,3) 1 (0,1 ) 4.0 2 0.6
Direction - - + + -

f42) or (F2.57) 5.64 0.61 7.36 16.83 (0.27)

P 0.060 NS 0.025 <0.001 NS

B ~ E R F LPOLLINATOR
Y SPECIES ABUNDANCE.-oVeT-
all abundance of butterfly pollinators did not differ
significantly among the three sites (Table 4), al-
though this result masks differences at the species
level. Abundance of A. ahmsoni and I: aecus in-
creased at D and M relative to U, while D. descom-
besi decreased. No difference in the abundance of
the occasional pollinator C. pomona was recorded,
and other occasional pollinators were observed too
infrequently for meaningful statistical analysis.
TREE
DENSITY,
SIZE,
A N D FLOWER AND FRUIT PRODUC-
TioN.-Density of D. obtusifolius within the nine
plots ranged from 24 to 41 trees/ha but there was
no significant difference in density or tree size
across sites (Table 5). Flower production between
sites and among trees within a site was similar (Ta-
ble 5; nested ANOVA on between site variance: F2
= 0.60, N.S.). Fruit production was also similar
across trees and there was no discernible site effect
(Table 5).
DISCUSSION
At Huay Kha Khaeng, extraction of S. siamensis
over recent decades has resulted in a marked in-
crease in understory flowering plant cover (Table
I), presumably in response to increased light pen-
etration in the more open disturbed habitats (Ka-
bakoff & Chazdon 1996, Ostertag 1998). The in-
crease in understory flowering plant cover implies
increased availability of understory floral nectar re-
sources at D. In particular, the invasive exotic C.
odorata, the most widespread herbaceous plant at v,
'(1
disturbed sites, presented large numbers of flowers rn
that were frequently visited by butterflies. In con- 0
trast, canopy floral resources were similar across the
three sites, as D. obtwifolius was the only common t
flowering tree during the study period and no dif- v,
ferences in its density, size, or flower production rn
(Table 5) across sites were recorded.
This shift in the relative abundance of floral
20
resources from the canopy to the understory at dis- z
turbed locations attracted butterfly pollinators of
D. obtusz@lius to the understory, resulting in low
diurnal pollinator activity on D. obtusifolius (Table
2 ) . Indeed, an earlier study showed that D. obtu-
sifoliw flowers at D that were visited by pollinators
were more likely to receive incompatible cross-spe-
cies pollen, indicating that these pollinators were
visiting other pollen sources in the understory
(these being the only alternative available) more
frequently (Ghazoul 2002b). Additionally, the
overall decrease in abundance of other (non-cano-

TABLE 5. Den+ size (diameter at breast height), andfEower andfiuit production of Dipterocarpus obtusifolius trees
at U, M and D. Density and size data deriurdjom three I ha plots at each site.

D. obtusifooliw D. obtusifoliw size Flowers per panicle Fruit per panicle

Site density (Nlha) DBH (cm t SE) (f t SE) (f t SE)

U 33.3 ? 4.1 31.7 t 1.8 4.06 2 0.07 1.06 t 0.03

M 30.0 t 3.1 32.9 t 1.4 4.16 t 0.06 1.08 2 0.04
D 29.0 t 2.6 28.3 t 1.0 4.11 t 0.06 1.12 2 0.04
162 Ghazoul

py) butterfly species at disturbed sites (Ghazoul early stage of development. In this respect, Delia
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 leabirds, visited fewer
D. obtusifoliw 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 Delia 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
Dipterocarpw obtustji2ius is also pollinated by to reduced fruit set following a decline or loss of
endothermic sphingid moths (Ghazoul 1997) that their principal pollinators (Johnson 1992, Rathcke
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
from the canopy. Light trap results indicated no pollinators (Ghazoul et al. 1998).
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. obtustjdius 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 (4Dudash & 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). Dipterocarpw obtusi- bution of forest floral resources and consequently
f i l i w 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
et a/. 1996).
A further implication of this study is that mon-
itoring the abundance of species that contribute to
mutualistic interactions may not be sufficient to
determine the state of those interactions. Rather,
monitoring changes in the processes mediated by
those interactions may improve predictions of fu-
ture community composition over those that ex-
trapolate from recent trends in local abundance.
Ecological processes, as the sum of multispecies in-
teractions, are more representative of forest resil-
ience and less sensitive to natural variability than
numerical assessments of species richness or pop-
ulation abundance. Indeed, process-orientated
measures are currently preferred for assessing the
maintenance of biodiversity in managed natural
forests (Didham et al. 1996, Ghazoul and Hellier
2001), and management strategies designed to con-
serve ecological processes are easier to devise and
have greater chance of success than strategies that
aim to conserve biodiversity directly (Lug0 1995).
ACKNOWLEDGMENTS
I am grateful for support from Mr. C. Pitdamkhan and
the staff of Huay Kha Khaeng Wildlife Sanctuary, Dr. C.
Hutacharern and K.Chaisurisri of the Royal Forest De-
partment, and J. Coles at the ASEAN Forest Tree Seed
Centre. Field research was conducted with the assistance
of N. Pornsurat, K. Liston, and A. Macgregor. Permission
to conduct research in Thailand was granted by the Na-
tional Research Council of Thailand.

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