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Asian weaver ants, Oecophylla Smaragdina, and their repelling of pollinators

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 Blackwell Science, LtdOxford, UKEREEcological Research1440-17032004 Ecological Society of Japan196669673Original ArticleAnt–pollinator interactionK. Tsuji
et al.

Ecological Research (2004) 19: 669–673

Asian weaver ants, Oecophylla smaragdina, and their repelling

of pollinators
Kazuki TSUJI,1,2,* Ahsol HASYIM,3 Harlion3 and Koji NAKAMURA4
1
Department of Biology, Faculty of Science, Toyama University, Toyama, 930–8555, Japan, 2Department of Environmental Sciences
and Technology, Faculty of Agriculture, University of the Ryukyus, Okinawa 903–0213, Japan, 3Research Institute for Fruit, PO Box
5 Solok, 2730, West Sumatra, Indonesia, and 4Ecological Laboratory, Faculty of Science, Kanazawa University, Kanazawa
920–1192 Japan

The Asian weaver ant, Oecophylla smaragdina, is known to have outstanding predatory power. This ant
can protect the host plants from attacks of phytophagous insects and therefore has been used for biological
control in the tropics. We present evidence for a possible negative effect of Oecophylla on the performance
of host plants. Our observation in a fruit orchard of rambutan in Sumatra suggested that the presence of
Oecohylla nests on the trees statistically significantly lowered the flower-visiting rate of flying insects,
involving the major pollinator Trigona minangkabau. The visiting rate of Oecophylla workers to each flower
shoot of rambutan significantly negatively correlated with the visiting rate of flying insects. Empirical
evidence of such an inhibitory effect on flower-visiting of pollinators cased by aggressive ants has been
scarce so far.

Key words: ant, interspecific interaction, Oecophylla, pollination, stingless bee

Introduction tion to the peculiar nesting behavior bonding leaves

together by their larval silk (Hölldobler 1983;
Ants are among the most dominant animals in terres- Hölldobler & Wilson 1990; Azuma et al. 2002). The
trial and arboreal ecosystems of the tropics and sub- Asian weaver ant, Oecophylla smaragdina, is known as
tropics, as the major scavengers and the predators on the ‘living pesticide’ utilized in biological control of the
many arthropods including themselves (Hölldobler & world earliest record in China (Konishi & Itô 1973;
Wilson 1990; Tobin 1991). However, they are often Hölldobler & Wilson 1990). In modern times, a number
mutualistic symbionts of plants such as Acacia and of ecologists, studying biological pest management in
Macalanga and other insects such as homopterans and the tropics, have tried to test such an economical value
licaenid butterflies, protecting them from natural ene- with rigorous scientific methods, and most of them have
mies and competitors to reword resources they provide suggested that the predatory power of Oecophylla is
such as foods and nest sites (Janzen 1966; Beattie 1985; most outstanding among ants in their localities (e.g.
Pierce 1989; Hölldobler & Wilson 1990; Fiedler 1991; Way & Khoo 1992; Peng et al. 1997, 1999; Van Mele
McKey et al. 1993). The effects of ants on abundance & Cuc 2000).
and survival strategies of other orgainsms are complex, The relationship between the weaver ants and their
usually depending on many factors that are often spe- nesting plants is facultative, as the ants use the leaves
cific to each case of interspecific interaction in each of almost any kind of plants including trees, herbs and
locality (McKey et al. 1993; Djieto-Lordon & Dejean grass (Hölldobler & Wilson 1990). Their possible effect
1999; Itioka et al. 2000; Bluthgen et al. 2003; Fleming on fitness of plants should exist in various ways. It can
& Nicolson 2003). Therefore, before working out a be positive as revealed by previous studies, since they
general picture on the roles of ants in local ecosystems, will remove herbivorous insects. While it can be
a major goal of insect ecology, we need to accumulate negative, because they often care for fluid-sucking
more empirical information on specific cases.
The weaver ants of the genus Oecophylla are one of
the most impressive members of forest landscapes in *Author to whom correspondence should be addressed. Email:
the Old Tropics because of their dominance in local tsujik@agr.u-ryukyu.ac.jp
habitats, large body size and the aggressiveness in addi- Received 29 March 2004, Accepted 21 June 2004.
670 K. Tsuji et al.
homopterans that damage the plants and indirectly
cause fungal diseases of the plants (Kalshoven 1981).
Furthermore, they might reduce the efficiency of pho-
tosynthesis of host plants by using leaves for nests and
by territorial markings on leafs with feces (Hölldobler
& Wilson 1978, 1990). In the economical point of view
there is an additional drawback, that is, their uncontrol-
lable aggressiveness can hinder efficient works in the
orchards (Kalshoven 1981). The overall ecological and
economical values of the weaver ants in tropical agro-
ecosystems are still the issue to be studied in details.
In the present study, we address the question on
another negative effect on plant fitness and on the com-
mercial value of domesticated plants: whether or not the
ants repel pollinators of host plants. The ‘ant plants’
Acacia zanzibarica and Acacia drepanolobium, which
have a close mutualistic association with ants such as
Crematogaster, are known to have a tactic solving the
dilemma that the partner will otherwise repel both her-
bivores and pollinators (Willmer & Stone 1997). Young
flowers of the plants release ant-repellent during the
short time of blooming. However, we predict that cul-
tivated plants with facultative relationship to Oecophylla
should have no such measure. We show that indeed the
presence of Oecophylla on rambutan (Nephelium lappa-
ceum) trees in a fruit orchard in West Sumatra markedly
reduces the frequency of visit of flying insects to their
flowers, while the presence of the other ants has no
significant negative effect on pollinator attraction. Such
an inhibitory effect on pollination cased by ants has
been supposed to exist (Bronstein 1988; Willmer &
Stone 1997), but has not been closely studied until
recently.
Methods
All field research was carried out in the experimental
orchard of the Research Institute for Fruits in Solok,
West Sumatra on 20 August 1998, when most of the
rambutan trees in the field were blooming. The obser-
vations were conducted between 8:00 and 9:40 a.m.
Sumatra time when the stingless bee Trigona minangk-
abau, the major pollinator in the study site (Inoue et al.
1985), were most actively visiting the flowers. We care-
fully selected six rambutan trees of similar size, located
within an area of 70 m radius; three had many Oeco-
phylla nests and the rest had none. Many Oecophylla
workers were walking on the plant-surfaces of the
former, while the weaver ant was almost absent in the
latter. Each of the three trees was occupied by each of
three distinct ant colonies that was checked by the test
of aggression in advance. In each tree we have chosen
six flower-shoots haphazardly, thus a total of 36 flower-
shoots were selected for the observation. In each flower-
Ecological Research (2004) 19: 669–673
shoot usually dozens of individual small flowers were
blooming. We observed each flower-shoot for 5 mins
when we recorded all visits of flying insects and ants.
‘Visited’ is defined as when the insect had direct contact
with a flower. Consecutive visits of the same individual
insect to the same shoot that consisted of multiple
‘touch and go’ were counted as one incidence. How-
ever, a revisit, after having lost track of the insect, might
have been counted as a new incidence. We assigned a
random sequence (1–12) for the order of trees. After
each of the first three authors (KT, AH and H)
observed one shoot for 5 min, they moved to a new tree
according to the random sequence. Thus each tree was
observed twice according to the random sequence by
each observer. As all the observers shared the same
sequence, each tree was subjected to a simultaneous
observation of three shoots at a given moment.
We compared the visiting rate of pollinators among
trees and among shoots with and without Oecophylla by
various statistical procedures. JMP 4J software (SAS
Institute, Cary, NC, USA) was used for all statistical
tests. No pesticide was used in the study site during
1998–1999.
Results
The visiting rate of Trigona per flower shoot statistically
significantly differed between trees with and without
Oecophylla nests, and on average the latter had more
visitors (Fig. 1). The number of Oecophylla workers
walking on a shoot, however, also differed among
shoots, even within the same tree. Approximately 80%
(16 of 18) of the flower shoots on the trees with Oeco-
phylla nests were visited by one or more workers of the
ants during the 5-min observation. This could be
explained as temporal variation by chance. Given such
temporal variation of the ant number, however, it is
possible that the negative effect on pollinator attraction
results only in the presence of the ant on the shoot. For
this reason we also compared the incidence of Trigona
visit to the shoots where at least one Oecophylla visited
during 5 min with that to the shoots where no
Oecophylla visited, regardless of the tree difference.
The result became much clearer. The presence of Oeco-
phylla workers on the shoot is negatively associated with
the visiting rate of Trigona (Fig. 2). An ANCOVA treating
each shoot as an independent unit also showed that the
visiting rate of Oecophylla statistically significantly neg-
atively correlated with the visiting rate of Trigona
(Table 1). A similar effect of Oecophylla was also
detected on the number of the other flying insects vis-
ited to the flower shoots (shoots with Oecophylla: n =
16, mean ± SD = 0.19 ± 0.413; shoots without Oeco-
phylla: n = 20, mean ± SD = 0.45 ± 0.945, Table 2).
Ecological Research (2004) 19: 669–673 Ant–pollinator interaction 671

Occasionally, workers of other ant species such as
Polyrachys spp. and Crematogaster spp., also visited
flower-shoots, although it was the case only for the trees
with no Oecophylla nest. The presence of those ants
did not seem to hinder the visit of pollinators (either
Trigona minangkabau or the other flying insects all
together), although we admit the limited sample size
(Tables 1 & 2).
Scale insects (species is unidentified) that attracted
Oecophylla workers existed on some shoots (N = 3). We
tested their possible negative effect on the flower-
visiting rate of flying insects by ANCOVA. Neither the
number of scale insects nor the interaction between
the number of scale insects ¥ the number of Oecophylla
workers visited had a statistically significant effect on
the visiting rate of fling insects (Tables 1 & 2). How-
ever, this result was also subject to small sample size.
Discussion
As predicted, the results suggest that Oecophylla hinders
the approach of the host tree’s follower visitors. Inter-
estingly, this flower-visitor repelling effect seems to be
conspicuous only in the weaver ant. The presence of
other tree-doweling ants such as Crematogaster spp. and
Polyrachys spp., seemed to have little or no effect
(Table 2). The observed clear effect of Oecophylla
should mostly be a reflection of its characteristic behav-
ior exhibiting strong territorial defence and aggression

Fig. 1. Mean number of Trigoma minangkabau workers visited

per 5 min per flower shoot (closed bar), and that of Oecophylla
smaragdina workers (open bar). Each tree was treated as the
independent unit, and the arithmetic mean value over six flower
shoots on the same tree (n = 3 with the tree with Oecophylla nests
and n = 3 trees without Oecophylla nest) was the variable used for
statistical tests. The error values are the standard deviations of
tree average. The difference in the visiting rate of Trigoma
minangkabau between trees with Oecophylla smaragdina nests and
those without the nest was statistically significant (t = 4.37, df4,
P = 0.012). (!), Trigona; ("), Oecophylla.
Fig. 2. Comparison of the average number of Trigona minangk-
abau visited per 5 min between shoots with at least one Oecophylla
worker visited and those with no Oecophylla workers visited. The
numerals in parenthesis denote sample size (no. shoots). The
difference was statistically highly significant (median test, c2 =
21.43, P < 0.0001).

Table 1 An analysis of covariance of the number of Trigona visiting flower shoots

Source Sum of squares d.f. Mean square F-value Probability
No. Oecophylla workers 0.654 1 0.654 4.97 0.035
No. Polyrachys sp.workers 0.161 1 0.161 1.23 0.279
No. Crematogaster sp. workers 0.334 1 0.334 2.54 0.124
No. other ants 0.005 1 0.005 0.04 0.853
No. scale insects 0.052 1 0.052 0.40 0.534
Tree 0.232 5 0.046 0.35 0.875
No. Oecophylla workers ¥ no. of scale insects 0.082 1 0.082 0.62 0.437
Error 3.153 24 0.131
All measures except ‘tree’, a categorical variable, are log10(x + 1) transformed to stabilize variance. ‘Tree’ was treated as a random factor, the rest being
fixed factors. The traditional method of moments (EMS) was used, because the restricted maximum likelihood method (REML) failed to obtain a
convergence to a solution.
672 K. Tsuji et al. Ecological Research (2004) 19: 669–673

Table 2 An analysis of covariance of the number of flying insects, excluding Trigona, visiting flower shoots
Source Sum of squares d.f. Mean square F-value Probability
No. Oecophylla workers 0.533 1 0.533 4.78 0.039
No. Polyrachys sp.workers 0.122 1 0.122 1.10 0.305
No. Crematogaster sp. workers 0.321 1 0.321 2.88 0.102
No. other ants 0.025 1 0.025 0.22 0.642
No. scale insects 0.071 1 0.071 0.67 0.434
Tree 0.340 5 0.068 0.61 0.692
No. Oecophylla workers¥ no. of scale insects 0.070 1 0.070 0.63 0.437
Error 2.673 24 0.111
All measures except ‘tree’, a categorical variable, are log10 (x + 1) transformed to stabilize variance. ‘Tree’ was treated as a random factor, the rest being
fixed factors. The traditional method of moments (EMS) was used, because the restricted maximum likelihood method (REML) failed to obtain a
convergence to a solution.

toward other animals (Hölldobler 1983; Hölldobler &
Wilson 1990). In fact, we have directly observed many
times that Oecophylla workers aggressed and repelled
Trigona and other insects approaching, but never
observed such aggression by other arboreal ants to
flower visitors. Although our field observation was car-
ried out only in the morning in order to focus the
influence on Trigona, we believe this behavioral process
also works in the rest of the time during a day, since
Oecophylla has no clear daily activity pattern, being
active day and night (K. Tsuji, unpubl. data). A similar
behaviorally mediated indirect effect caused by the ant,
Crematogaster scutellaris, on the fig-fig wasp system has
recently been reported (Schatz & Hossaert-McKey
2003). In this case, the ants on the fig tree do not repel
the pollinator wasps but intensively prey on them. This
and our studies suggest certain arboreal ants actually
negatively interact with pollinators’ performances.
There is another explanation for the low visiting rate
of flower-visitors in the presence of Oecophylla: chemi-
cal inhibition, for example, territory marking phero-
mones known in Oecophylla (Hölldobler 1983) can also
work as insect repellents. This possibility is to be tested
in the future.
We have no quantitative datum about the ant effect
on real pollination success of the rambutan trees, since
we did not follow each shoot until fruiting (we admit-
tedly need such data). However, all three rambutan
trees with Oecophylla nests yielded fruits seemingly nor-
mally in December 1998, the harvesting season directly
following the observation (K. Tsuji & A. Hasyim,
unpubl. data), suggesting that the observed inhibitory
effect might not be economically important. Although
the ants lowered the frequency of pollinator visits, it
might be still high enough to receive sufficient pollens
for the pistils of the flowers. Another possibility is that
Oecophylla itself is a pollinator particularly mediating
selfing, as has been suggested in other ant-plant
associations (e.g. Kawakita & Kato 2002; Raju &
Ezradanam 2002). Future studies should test this
hypothesis, although literature suggests this unlikely,
because ants often damage pollen activities by their
external glands secretions (e.g. Hölldobler & Wilson
1978; Beattie et al. 1985; Bernardello et al. 2001; Galen
& Butchart 2003).
Despite the economical insignificance discussed ear-
lier, in an ecological point of view the effect of the ants
on their host plants can be significant. Hence, rambutan
followers have both male and female functions; the
effect of the limited pollinator visit on plant fitness
might differ between sexes. In general, male reproduc-
tive success (pollen donation in plants) is usually a
positive function of mating success, while increasing the
number of mates does not always enhance female
reproductive success (seed production in plants)
(Birkhead 2000). Therefore, if the observed pollinator-
repelling by Oecophylla would lead to lowered host
plant fitness, it should occur more prominently in the
male function, that is, the pollen donation. We need
further quantitative studies to test this idea and to
understand this interspecific interaction system. Future
studies should particularly focus pollen dispersal of
Oecophylla’s host plants.
Acknowledgements
We thank Kyosuke Ohkawara, Seigo Higashi for their
comments on an earlier manuscript. This study was
supported in part grant-aid from the Japan Ministry of
Education, Science and Culture (13640626 and
14405036).
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