Oecophylla longinoda (Hymenoptera:
Formicidae) as a biological control agent for
cocoa capsids (Hemiptera: Miridae)
P.M. van Wijngaarden, M. van Kessel & A. van Huis
Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH
Wageningen, The Netherlands, E-mail: [email protected]
The biology and ecology of the ant Oecophylla longinoda (Hymenoptera:
Formicidae) was studied in cocoa plantations in Ghana in 2005. The
main focus was the possibility to use the ant as a biological control
agent against capsids (Hemiptera: Miridae) which are important cocoa
pests. The effectiveness of both red and black strain O. longinoda to
control this pest was studied by relating its presence, abundance and
number of nests to canopy defoliation and percentage of pods damaged.
In total 300 cocoa trees in three different cocoa fields at the Cocoa
Research Institute of Ghana premises were examined. Both the presence of red O. longinoda and a high abundance of the ants were correlated with a thick canopy. This might be the result of either decreased
defoliation (lower capsid damage through protection by the ants), a
preference of the ants for thick canopies, or a relational combination of
both. The percentage pod damage (24) in trees with high ant abundance
was significantly lower than those in trees without ants (42). The number of pods damaged was about 50% lower for trees with black strain O.
longinoda compared to trees without ants. This reduction in capsid damage by black O. longinoda might be explained by its high aggressiveness.
The ant and especially the black strain is therefore considered a potential biological control agent of capsids. However, it seems that ant
abundance need to be high such that ants are not only present in the
tree canopy, but also cover the trunk where the vulnerable cocoa pods
are situated. The ant’s role in an integrated pest management strategy
should be further investigated, in particular its combination with the
natural pesticide neem.
Keywords: Oecophylla longinoda, weaver ant, capsid damage, biological
control, integrated pest management, Convergences of Sciences,
Ghana, cocoa
The ‘Convergences of Sciences’ (CoS) project initiated from the idea that scientific innovations arerarely used by farmers and that its contribution to poverty
alleviation is sub-optimal. It is believed that convergence is needed in technoloPROC. NETH. ENTOMOL. SOC. MEET. - VOLUME 18 - 2007
21
BIOLOGICAL CONTROL
gy development, not only between natural and social scientists, but also between
societal stakeholders (including farmers) and scientists. Of key importance
within the CoS principle is that societal stakeholders influence scientists’
research agendas and vice versa (democratization of science), and also that farmers gain more confidence in their own knowledge and capacities (farmer empowerment) (Röling et al. 2004). During the CoS project farmers came up with the
idea to use the weaver ant Oecophylla longinoda Latr. (Hymenoptera: Formicidae)
as a biological control agent against capsids (Hemiptera: Miridae) in cocoa
(Ayenor et al. 2004). Ayenor (2006) showed that the capacity of the ants to suppress capsids was equally effective as the use of the botanical pesticide neem.
Oecophylla longinoda (Hymenoptera: Formicidae) is the African variant of the
Oecophylla family and occurs in most tropical areas of Africa. The ants inhabit
tree canopies in which they build nests out of living leaves. Their feeding behaviour is generalistic (Way 1954, Vanderplank 1960) and Oecophylla is relatively
dominant compared to other ant species (Bigger 1981). Colonies might cover
large areas, occupying a number of tree canopies. The ants inhabit several crops
such as cocoa, coffee and citrus (Van Mele & Cuc 2003). Oecophylla smaragdina
(Fabr.), the Asian congener of O. longinoda, has already been used for centuries
to protect crop harvests in South-East Asia (Van Mele & Cuc 2000). Since several studies have shown significant reduced pest damage by O. smaragdina in for
example citrus plantations in Vietnam (as reviewed in Van Mele & Cuc 2003)
and mango (Peng & Christian 2004, 2005a, b) and cashew orchards (e.g. Peng et
al. 1999, 2001) in Australia, it is considered a good biological agent. Therefore,
this study focused on the possibility to use O. longinoda in an integrated pest
management strategy for cocoa.
Pods, the fruits of the cocoa tree containing cocoa beans, are mainly located
at the trunk of the tree, from the base up to the canopy. Capsids attack these
pods, which serve them as a source of food. The most abundant capsid species,
Salbergella singularis (Hagl.), Distantella theobroma (Dist.) and Helopeltis species
(as reviewed in Brun et al. 1997, Entwistle 1972), create lesions by injecting their
stylets into the husk of the pod. These lesions are by itself relatively harmless,
but they mediate infection of the pods by pathogenic fungi. Of these fungi,
Phytophthora megakarya is the most common one, causing the pod to die and turn
black (black pod disease) (Opoku et al. 2002). However, capsids not only attack
pods, but also feed on the young shoots called cocoa tree ‘chupons’. Infection of
shoots and branches by fungi is believed to cause dieback, resulting in defoliated trees (Entwistle 1972).
The purpose of this research was to give an alternative for the mass spraying
of capsids with synthetic pesticides provided gratuitously by the Ghanaian government. The aim is to contribute to a more environmental friendly way of pest
suppression with virtually no costs. In addition, the price farmers get for the
cocoa could increase, both because of better quality when pesticides are not used,
22
P.M. VAN WIJNGAARDEN, M. VAN KESSEL & A. VAN HUIS
as the bonus companies are willing to pay for organic cocoa. We conducted a
number of studies with the intention to enhance the effectiveness of the weaver
ant in pest control. These studies involved issues such as the possibility to introduce O. longinoda nests, effectiveness of pest suppression, nest composition, population dynamics and food consumption. The main question was whether or not
O. longinoda populations would be able to reduce capsid damage. Therefore, an
experiment was carried out to link ant presence and abundance with capsid damage.
MATERIALS AND METHODS
The experiments were carried out in three cocoa plantations at the Cocoa
Research Institute of Ghana premises at Tafo (Ghana). All the plantations had not
been sprayed with pesticides for the past season and no other experiments had
taken place which could have had an effect on both O. longinoda and capsid populations. In six different periods between the 6th of June and the 24th of October
in 2005, 50 trees were selected for examination, resulting in a total of 300 trees.
The trees were randomly chosen in plots of 10 by 10 trees.
Monitoring ant presence
Ant presence and abundance
For every selected tree the presence of the black or red strain of O. longinoda was
registered. Ant abundance was monitored by careful observation of the canopy
and trunk, using a ladder if necessary. Four scoring levels were used: no O. longinoda present on the tree (0); few ants observed on only one or two branch(es) (1);
ants observed on several branches of the tree (2); and many ants observed on
many branches of the tree and/or trunk (often many trails present) (3).
Nest counting
The number of nests per tree was recorded by carefully examining the tree
canopy. Since in some cases it was not possible to determine the exact number
of O. longinoda nests in the tree canopy (e.g. in cases of a very big or dense
canopy) often an estimate of the number of nests was made, based on ant trails
and ant abundance.
Monitoring capsid damage
Canopy
The Hammond index (Johnson & Burge 1971) is commonly used to estimate the
percentage of canopy loss due to capsid damage. This index represents five levels for estimating canopy loss (0: no damage to the foliage, 1: 0-25% damage to
the foliage, 2: 26-50%, etc.). A variant involving 21 levels was designed to estimate
differences in canopy loss with a margin of less than 10%: no damage to the
foliage (1); 1-5% damage to the foliage (2); 6-10% damage to the foliage (2); etc.
23
BIOLOGICAL CONTROL
Pods
All pods above the size of a human thumb were checked for presence of capsid
lesions. Only pods located less than four meters from the ground were included.
Pods located above this four meter level could not be reached for, and were therefore not examined. The total number of pods was documented together with the
number of pods with capsid lesions. With these data, the percentage of damaged
pods per tree was calculated.
Chupons
It was recorded whether chupons showed capsid damage. These observations
will be discussed.
Data analysis
The correlation between nest and ant abundance was tested with the Spearman
test. To investigate ant-capsid correlations all variables were linked in either a
univariate analysis (Mann-Whitney U test) or a multivariate analysis (KruskalWallis). To determine interrelated differences, post hoc tests were run. All tests
were carried out at the 0.05% confidence level.
Capsid presence and damage was also evaluated for different ant densities. A division was made between red and black O. longinoda to distinguish the effect of the different strains. To be able to compare the data of red and black O. longinoda for similar ant densities, an analysis was carried out only for trees with high ant abundance
(index 3). At last, the number of ant nests was correlated with capsid damage.
RESULTS
Canopy condition
There was no relation between ant presence in general and condition of tree
canopies (Table 1). When canopy thickness is correlated with ant abundance,
only trees with a high abundance of ants (index 3) had significantly higher leaf
coverage compared to those with no ants (index 0). The abundance of the red ant
strain is positively correlated with greater canopy thickness, whereas this does
not hold for the black strain of O. longinoda. A higher number of nests per tree
does not mean significantly less capsid damage. The nests were found to be in
places with low canopy cover.
Pod damage
The presence of O. longinoda is significantly correlated with lower pod damage
(Table 1, Fig. 1). Further, analyses show that pod damage is only significantly
lower when O. longinoda is present in high numbers. When only trees with high
ant abundance (index 3) are compared to trees with no ants (index 0), the pod
damage is significantly less (approximately 60%). However, a higher number of
O. longinoda nests is not significantly related to the level of pod damage.
24
0
0
0
0
9.1 (N=92)
9.1 (N=92)
9.1 (N=92)
9.1 (N=92)
9.1 (N=169)
+
1
R
R
1-4
Significant difference
between2
Ant presence
Ant abundance
Ant strain
Ant strain (for abundance 3)
Number of nests
Canopy index
8.6 (N=208)
MW: ns
8.8 (N=46)
2
8.9 (N=54)
3
8.3 (N=108)
KW: 0 & 3
8.3 (N=132)
B
9.1 (N=72)
KW: 0 & R
7.9 (N=59)
B
8.9 (N=45)
KW: 0 & R
8.0 (N=85)
>4 7.6 (N=46)
KW: 0 & 1-4; 0 & >4
Pods damaged (%)
Ant presence
41.7 (N=68)
+ 28.7 (N=170)
MW: – & +
Ant abundance
0 42.1 (N=67)
1 39.2 (N=32)
2 30.9 (N=43)
3 24.0 (N=96)
KW: 0 & 3
Ant strain
0 42.1 (N=67)
R 32.6 (N=111)
B 17.5 (N=56)
KW: 0 & B; R & B
Ant strain (for abundance 3)
0 42.1 (N=67)
R 25.9 (N=54)
B 16.2 (N=38)
KW: 0 & B; 0 & R
Number of nests
0 35.8 (N=117)
1-4 26.9 (N=79)
>4 33.4 (N=42)
KW: ns
1Presence: – = absent, + = present; abundance index: 1, 2 and 3; strain: R = red, B = black, N = number of trees; 2P ≤ 0.05 (MW = Mann-Whitney U test,
KW = Kruskal-Wallis test); ns = not significant
Ant indices1
Table 1. Effect of the ant Oecophylla longinoda on preventing capsid damage to the canopy and to pods in cocoa (average values)
P.M. VAN WIJNGAARDEN, M. VAN KESSEL & A. VAN HUIS
25
BIOLOGICAL CONTROL
Figure 1. The effect of the ant Oecophylla longinoda on pod damage by capsids per cocoa
tree (%). A = Trees without, and with red or black ants. B = Trees without, and with
red or black ants (no ants and abundance level 3 only). C = Trees with different ant
abundances.
When a division is made between different strains, it appears that only for
trees with black ants the pod damage is significantly lower (approximately 50%)
compared to trees without ants. Red O. longinoda ants lower pod damage, but not
significantly.
Chupon damage
When O. longinoda was present in a tree, it was often observed that young
chupons had many ant trails on them. If a tree had many chupons and O. longinoda was present, the ants often nested in the chupon foliage. When O. longinoda
was present the chupons hardly showed any capsid damage.
DISCUSSION
Canopy condition
The relation between ant occurrence and canopy thickness might have two reasons. It is possible that trees with high O. longinoda abundance and high numbers
of nests have a thick (healthy) canopy because of reduced capsid damage by ants.
Another reason might be that O. longinoda has a preference for healthy canopies
for both environmental and ecological reasons. However, it is difficult to sort
out these causal relationships. Another possibility is an interaction between both
systems: a thick canopy attracts ants and due to the higher number of these predators the canopy is better protected against capsids. This is a self reinforcing
process: the canopy gets thicker as a result of reduced capsid damage and thus
attracts more O. longinoda, etc. Abundance of red O. longinoda correlates better
with increased canopy coverage than abundance of the black strain does. We
have no explanation for this difference between the two strains.
26
P.M. VAN WIJNGAARDEN, M. VAN KESSEL & A. VAN HUIS
As ant abundance, the number of their nests is also related to canopy cover.
Although the same explanation could be given as above, it is also likely that ants
choose trees with a thick foliage as the habitat conditions are more favourable
for nesting. This could be based on two reasons: either statistically there is a
higher chance of finding a suitable nesting site in a thicker canopy, or they
choose a thicker canopy to provide nesting sites for seasonal migration, which is
suggested in the literature and by farmers (Way 1954, Vanderplank 1960). The
fact that nests do not remain at one location during the year was supported by
observations of colony movement for over more than three meters to other trees.
Also farmers had depicted the seasonal movement of ants over their plantation.
In addition to observations in literature (Way 1954, Vanderplank 1960) our own
observations confirm that nests of O. longinoda were often found on the outside
of the canopy in direct sunshine. Besides that, nests were observed in trees with
a serious degree of defoliation.
Pod damage
Lower pod damage (approximately 50%) was observed in trees with black O.
longinoda present compared to trees without ants. This indicates that this ant
strain could be a good biological control agent of capsids. However, it is not sure
whether the same results would be achieved when replicated in cocoa fields having different environmental conditions.
Abundance of weaver ants might be very important in cocoa pest management. Pods mainly grow on the trunk and it is likely that these pods will only
be protected against capsids if the ants also occur at the trunk and not only high
up in the canopy, which seemed to be their preferred territory. The ant was only
observed on the trunk of a tree if the ant population on that specific tree was
high (index 2 or 3). If abundance was very low ants often only occurred in the
top and/or middle part of the canopy. Therefore, in order to protect cocoa pods,
O. longinoda populations have to be very abundant, whichis also suggested by
Vanderplank (1960). Other studies should focus on whether O. longinoda colonies
could protect a whole plantation in a sufficient manner. Naturally most weaver
ant colonies do only cover part of it (Peng & Christian 2005b). Black O. longinoda colonies were observed to vary in concentration: parts of the plantations were
highly occupied, where as other parts were not occupied at all. This could indicate that only parts of the plantation with a high ant occupation are protected.
The reason for the efficiency of black O. longinoda in controlling capsids
might be due to its aggressiveness. Several observations in the fields have shown
that in case of disturbance or danger, black ants attack immediately whereas ants
of the red strain tend to keep a distance. In case of encountering capsids, black
ants always succeeded to catch the prey where as red ants often led it slip away.
However, these are just observations and a study should be done in order to confirm the reason for differences in efficiency. Besides, it might be important to
know what exactly determines differences in strains, since it was sometimes
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BIOLOGICAL CONTROL
observed that the two strains were part of one and the same colony; also intermediate forms were found. It has been suggested that this is due to differences
in diet: red O. longinoda would often mainly feed on honeydew produced by
Homoptera; where as the black ants are more active predators (Vanderplank
1960). This would also explain why black O. longinoda reduces capsid damage to
a greater extent than red strain populations.
Though not significant, the results indicate a decreasing percentage of damaged pods with an increasing number of ant nests.
Chupon preference
Observations in the field indicate that O. longinoda ants possibly prefer chupons
above other branches in the canopy for nest building. This might be because
chupons often have numerous big fresh leaves which possibly match the optimal
conditions for nest building activities (Way 1954, Van Mele & Cuc 2003).
Chupons are often very vulnerable for infestation of capsid lesions. Protection
of chupons would be an extra advantage of the use of O. longinoda in cocoa pest
control.
Integrated pest management
The 50% reduction in capsid damage by black O. longinoda is considerable, but it
may be questioned whether this is sufficient or not. Farmers perceive pesticides
use to be effective. However, synthetic pesticides also wipe out ant colonies. It
remains to be seen whether O. longinoda can suppress capsids sufficiently, taking
into account that according to Entwistle (1972) only a few capsids can already
have a devastating effect on cocoa trees. However, the method could be effective
when used over a longer period. The method also does not pose any harm to the
environment. Besides, it has low initial costs, does not require much labour, and
farmers are already convinced of O. longinoda’s usefulness.
Sporleder & Rapp (1998) showed that palm trees with O. longinoda had significantly higher numbers of coconuts (resulting in higher yield) than those without. In studies of Peng and his co-workers the number of nuts was positively
linked to O. longinoda population stability as well as fruit quality (Peng et al.
1998, 1999, Peng & Christian 2005b). It would be a valuable experiment to look at
cocoa yield (such as number of pods, number of beans, bean weight, and quality) in relation to O. longinoda presence and population stability.
This study indicates that for successful biological pest control, O. longinoda
could be part of an integrated pest management strategy, including other components such as black pod removing, weeding and pruning. Therefore, ants should
be introduced in plantations where they are absent and reinforced in plantations
where ant abundance is low. Introduction of ants is an option (Van Mele & Cuc
2003), although other experiments within this research indicated some difficulties
like hostile native O. longinoda colonies (Peng et al. 1999, Van Mele & Cuc 2003),
other competing ant species (Greenslade 1972, Peng et al. 1999, Way & Khoo 1992,
28
P.M. VAN WIJNGAARDEN, M. VAN KESSEL & A. VAN HUIS
Peng & Christian 2005b) and failure of large scale introduction, which could also
partly be the result of the first two reasons. Further research should focus on
improvement of the introduction method and overcoming its basic problems.
Human intervention (so called ‘ant husbandry’) might be needed for O. longinoda colonies to grow out to be an effective biological control agent. A detailed
description of introduction methods and ant husbandry is found in Van Mele &
Cuc (2003). An addition to the IPM strategy including ant husbandry could be the
use of the botanical pesticide neem. According to own experiments neem, applied
directly on or in the surroundings of O. longinoda nests or individuals, has no
direct deterrent effect or affect mortality rate. Neem was also included in the
IPM strategy of the CoS project (Ayenor 2006, Dormon 2006).
The suggestion of using ants in pest control came from the farmers themselves.
This increases the chance of adoption of the method by farmers. A few objections
were raised, but all problems mentioned by farmers were easily resolved, even
after discussions among themselves. What is needed is an easy, cost-effective and
non labour-intensive method of introducing and maintaining O. longinoda populations in cocoa plantations. Besides that, the advice should be mediated to the farmers, for example through farmers fields schools (FFS). To facilitate this process, a
leaflet with basic information accompanied the report of this study.
One of the greatest difficulties of introducing biological control using ants,
are the free mass spraying activities. However, these mass sprayings are believed
to stop in the near future (E.N.A. Dormon, personal communication). When
farmers are forced to pay for capsid control, they will look for the most suitable
method, which should both be cheap and effective. The use of O. longinoda, if
necessary in combination with neem or other biological measurements, might
provide the most convenient alternative.
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