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: machiel.vanwijngaarden@wur.nl
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 pres-ence of red O. longinodaand a high abundance of the ants were correlat-ed with a thick canopy. This might be the result of either decreascorrelat-ed 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 num-ber of pods damaged was about 50% lower for trees with black strain O. longinodacompared to trees without ants. This reduction in capsid dam-age by black O. longinodamight be explained by its high aggressiveness. The ant and especially the black strain is therefore considered a poten-tial 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 scien-tific innovations arerarely used by farmers and that its contribution to poverty alleviation is sub-optimal. It is believed that convergence is needed in
technolo-Formicidae) as a biological control agent for
cocoa capsids (Hemiptera: Miridae)
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 farm-ers gain more confidence in their own knowledge and capacities (farmer
empow-erment) (Röling et al.2004). During the CoS project farmers came up with the
idea to use the weaver ant Oecophylla longinodaLatr. (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
sup-press capsids was equally effective as the use of the botanical pesticide neem. Oecophylla longinoda(Hymenoptera: Formicidae) is the African variant of the Oecophyllafamily and occurs in most tropical areas of Africa. The ants inhabit tree canopies in which they build nests out of living leaves. Their feeding
behav-iour is generalistic (Way 1954, Vanderplank 1960) and Oecophyllais 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
sev-eral studies have shown significant reduced pest damage by O. smaragdinain 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 megakaryais 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 defoliat-ed 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 gov-ernment. 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,
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
intro-duce O. longinodanests, effectiveness of pest suppression, nest composition,
pop-ulation dynamics and food consumption. The main question was whether or not O. longinodapopulations would be able to reduce capsid damage. Therefore, an experiment was carried out to link ant presence and abundance with capsid dam-age.
MATERIALS AND METHODS
The experiments were carried out in three cocoa plantations at the Cocoa
Research Institute of Ghanapremises 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. longinodaand capsid
pop-ulations. In six different periods between the 6thof June and the 24thof 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. longinodawas
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.
longin-odapresent 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 lev-els 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
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 there-fore 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 (Kruskal-Wallis). 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
divi-sion was made between red and black O. longinodato distinguish the effect of the
dif-ferent strains. To be able to compare the data of red and black O. longinodafor
simi-lar 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. longinodais significantly correlated with lower pod damage
(Table 1, Fig. 1). Further, analyses show that pod damage is only significantly
lower when O. longinodais 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. longinodanests is not significantly related to the level of pod damage.
Table 1.
Effect of the ant
Oecophylla
longinoda
on preventing capsid damage to the canopy and to pods in cocoa (average values)
Ant indices 1 Significant dif ference between 2 Canopy index Ant presence -9.1 (N=92) + 8.6 (N=208) MW : ns Ant abundance 0 9.1 (N=92) 1 8.8 (N=46) 2 8.9 (N=54) 3 8.3 (N=108) KW : 0 & 3 Ant strain 0 9.1 (N=92) R 8.3 (N=132) B 9.1 (N=72) KW : 0 & R
Ant strain (for abundance 3)
0 9.1 (N=92) R 7.9 (N=59) B 8.9 (N=45) KW : 0 & R Number of nests 0 9.1 (N=169) 1-4 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=1 11) 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=1 17) 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-W
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. longinodaants 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.
longin-odawas 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
rea-sons. It is possible that trees with high O. longinodaabundance and high numbers
of nests have a thick (healthy) canopy because of reduced capsid damage by ants.
Another reason might be that O. longinodahas 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 pred-ators 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. longinodacorrelates better
with increased canopy coverage than abundance of the black strain does. We have no explanation for this difference between the two strains.
Figure 1.The effect of the ant Oecophylla longinodaon 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.
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. longinodawere 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 hav-ing different environmental conditions.
Abundance of weaver ants might be very important in cocoa pest manage-ment. 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. longinodacolonies
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.
longino-dacolonies were observed to vary in concentration: parts of the plantations were
highly occupied, where as other parts were not occupied at all. This could indi-cate 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 con-firm the reason for differences in efficiency. Besides, it might be important to know what exactly determines differences in strains, since it was sometimes
observed that the two strains were part of one and the same colony; also inter-mediate 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. longinodareduces capsid damage to
a greater extent than red strain populations.
Though not significant, the results indicate a decreasing percentage of dam-aged pods with an increasing number of ant nests.
Chupon preference
Observations in the field indicate that O. longinodaants 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. longinodain cocoa pest
control.
Integrated pest management
The 50% reduction in capsid damage by black O. longinodais 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. longinodacan 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. longinodahad
signif-icantly higher numbers of coconuts (resulting in higher yield) than those with-out. 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
quali-ty) in relation to O. longinodapresence 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 compo-nents 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. longinodacolonies (Peng et al.1999, Van Mele & Cuc 2003),
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.
longino-da 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
popula-tions in cocoa plantapopula-tions. Besides that, the advice should be mediated to the farm-ers, 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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