TheIndonesian potential Journal of artificial of Agriculture nesting sites 3(1), ... 2010: 45-50 45

THE POTENTIAL OF ARTIFICIAL NESTING SITES FOR INCREASING THE POPULATION DENSITY OF THE BLACK CACAO

Meldy L.A. Hosanga), Christian H. Schulzeb), Teja Tscharntkec), and Damayanti Buchorid)

a)Indonesian Coconut and Other Palmae Research Institute, Jalan Bethesda II, Mapanget PO Box 1004, Manado 95001, North Sulawesi, Phone: (0431) 812430, 851430, Facs.: (0431) 812017, Email: [email protected] b)Department of Ecology I, University of Bayreuth, D-95440 Bayreuth, Germany c)Agroecology, University of Göttingen, Waldweg 26, 37073 Göttingen, Germany d)Department of Plant Pests and Diseases, Faculty of Agriculture, Bogor Agricultural University, Kampus IPB Darmaga, Bogor 16680, West Java, Indonesia

ABSTRACT In Indonesia, biological control of the mirid bug by introducing the black cacao ants was first documented in The black cacao ( thoracicus Smith) the early 1900s. There were large signboards on the main (: Formicidae) is one of the predators commonly roads of the Siloewok Sawangan estate (Central Java), at found in cacao plantations and known to be an effective biological the time it was the largest cacao estate in Java, saying control agent of cacao pests. One of the limiting factors for the population density of the ants in cacao plantations may be the without black ants no cacao (Giesberger 1983). This availability of adequate nesting sites. The purposes of this study emphasizes the importance of ants in controlling cacao were to evaluate which artificial nesting sites are most successful in pests, but this practice was discontinued as pesticides attracting black cacao ants and in which nesting sites of D. became widely available (Perfecto and Castineiras 1998). thoracicus colonies reach the largest size. The study was conducted More studies on D. thoracicus were conducted in Malaysia in two cacao plantations in the vicinity of the Makmur village in the 1980s. Studies by Khoo and Chung (1989) and Way located at the eastern margin of the Lore Lindu National Park, Palolo valley, Central Sulawesi. At each cacao plantation, 20 trees and Khoo (1989) showed that the black cacao ants could colonized by black cacao ants were selected. In every chosen tree, protect cacao pods against Helopeltis sp. Furthermore, all five nest types were placed for two weeks. D. thoracicus See and Khoo (1996) reported that an increasing significantly preferred artificial nesting sites constructed of bundles abundance of the black cacao ants was associated with a of dry coconut leaflets. Other artificial nests (bundles of dry banana significant reduction of the percentage of unextractable and cacao leaves, hollow bamboo filled with dry leaves, and plastic bags filled with dry cacao leaves) did contain colonies with less pods (all beans stuck to each other and to the husk). They adult ants, larvae, and pupae. also found that the percentage of pods infested by C. cramerella was generally below 50% in plots with a high [Keywords: , Theobroma cacao nesting, ant abundance of D. thoracicus and mostly exceeded the biological control] 50% level in plots where these ants were scarce. While in many plantations the black cacao ant is extremely rare; in some plantations it does not occur at all. INTRODUCTION To study if nesting site was an important limiting factor for

Biological control by using natural enemies such as parasitoids, predators, and pathogens has gained more interest in the last ten years. The use of ants for controlling insect pests was first reported from China (Flint and van den Bosch 1981; Hölldobler and Wilson 1990). The black cacao ant (Dolichoderus thoracicus Smith) (Figure 1) is one of the well-known predators that has a high potential to act as biological control agent against cacao pests. The ant is capable of decreasing pod damage caused by mirid bugs of the Helopeltis sp. and the cacao pod borer (Conopomorpha cramerella Snellen) (Giesberger 1983; Khoo and Chung 1989; Way and Khoo

1989; Khoo and Ho 1992; See and Khoo 1996; Khoo 2001) Figure 1. Black cacao ant (Dolichoderus thoracicus) attending and also can protect cacao trees against folivorous white meally bugs (Cataenococcus hispidus Marrison) (Hosang 2004). on the surface of a cacao pod. 46 Meldy L.A. Hosang et al. the abundance of D. thoracicus, five different kinds of bundle of dry coconut leaflets; (2) Ban = bundle of dry artificial nesting sites were placed in two cacao plantations. banana leaves; (3) Cac = bundle of dry cacao leaves; (4) In particular, the purposes of this study were to evaluate Bam = bamboo (length: 25 cm, diameter: 10 cm) filled with which artificial nesting sites were most successful in dry cacao leaves; and (5) Bag = transparent plastic bag attracting black cacao ants and in which nesting sites D. filled with dry cacao leaves thoracicus colonies reach the largest size. At both cacao plantations, 20 trees colonized by black cacao ants were selected (2 x 20 trees = 40 trees). In every tree all five nest types were placed to black cacao ants by MATERIALS AND METHODS tying the artificial nests on the trunk or main branch of tree (2 x 20 nests per nest type = 40 nests per nest type; 40 The study was conducted at the eastern margin of the nests x 5 nest types = total of 200 nests). Due to this Lore Lindu National Park in Palolo valley, Central Sulawesi. experimental design, the ants had the possibility to choose The two selected cacao plantations, Makmur 1 (S 01°08.29' between the different nest types in every tree (Figure 2). E 120°03.22') and Makmur 2 (S 01°08.28' E 120°03.34'), were After exposing all nests for 2 weeks, they were located in the vicinity of the Makmur Village (Palolo Sub- recollected from the trees and the size of the established district, Donggala District) at an altitude of 620 and 610 m colonies was quantified for all nests by counting the asl, respectively. number of adult ants, larvae, and pupae. Additionally, D. The study was conducted in October 2002 thoracicus ants active at the tree trunks of 1.0-1.5 m above synchronously at both selected study sites, Makmur 1 ground and on the leaves and branches of the lower canopy and Makmur 2. In both cacao plantations, five different were counted or estimated for all treated trees and trees kinds of artificial nesting sites were placed, i.e. (1) Coc = nearby which were not equipped with artificial ant nesting

Figure 2. Artificial nesting sites placed to black cacao ants: bundle of dry coconut leaflets (top left), bundle of dry banana leaves (top center), bundle of dry cacao leaves (top right), plastic bag filled with dry cacao leaves (bottom left), and bamboo filled with dry cacao leaves (bottom right). The potential of artificial nesting sites ... 47

123 sites but colonized naturally by black cacao ants. Therefore, 100 Makmur 1 123 Makmur 2 123

123 123 for each studied plantation, 20 pairs of trees colonized 123 123

80 123 123 with black cacao ants but with and without artificial ant 123 123 123 123

123 123 123 nests are available for comparison. 60 123 123 123 123

123 123 123 123

One-way analysis of variance (ANOVA) was used to 123 123 123 123 123

123 123 123 123 123 40 123 123 123 123 123 analyse effects of artificial nest types on colonization 123 123 123 123 123

123 123 123 123 123 success and colony size of the black cacao ants. Scheffé 123 123 123 123 123 20 123 123 123 123 123 test was applied to compare the population of black cacao 123 123 123 123 123 123 123 123 123 123

123 123 123 123 123

123 123 123 123 123

ants on trees with and without artificial nests. The program Colorization rate (%) 0 Statistica 5.5 (StatSoft 1999) was used to perform all Coc Ban Cac Bam Bag statistical analyses. Means were given ± standard devia- Artificial ant nest tion. Figure 3. Colonization rates of Dolichoderus thoracicus on different types of artificial nesting sites placed in RESULTS AND DISCUSSION two cacao plantations (Makmur 1 and Makmur 2) in cacao trees already occupied by D. thoracicus; Coc = bundle of dry coconut leaflets, Ban = bundle of dry Effect of Type of Nesting Sites on Colonization banana leaves, Cac = bundle of dry cacao leaves, Success Bam = bamboo filled with dry cacao leaves, and Bag = transparent plastic bag filled with dry cacao leaves. Black cacao ants colonized all types of artificial nesting sites placed in cacao trees, but the five types of nests differed in respect to their colonization rate. In Makmur 1, D. thoracicus colonized all (100%) Coc nesting sites. In p < 0.0001; Makmur 2: F4,15 = 9.10, p < 0.0001). In Makmur 1, respect to their colonization rate, the remaining four types significantly more queens were counted in Coc and Ban of nesting sites were ranked in the following sequence: nests compared to Bam and Bag nests. Cac nests did not Ban (83.75% of placed nesting sites colonized), Cac differ from other artificial nesting sites. In Makmur 2, (78.75%), Bam (60.00%), and Bag (36.25%). A similar significantly more queens were recorded in Coc nests than ranking of nesting sites was found at Makmur 2, although that in all other types of artificial nesting sites (Figure 5). lower colonization rates were found on Coc (88.5%), Ban The number of ant larvae at both study sites differed (63.75%) and Cac (58.75%), and a higher percentage of significantly between the placed artificial nesting sites Bam (83.75) and Bag nesting sites (46.25%) were colonized colonized by D. thoracicus (one-way ANOVA; Makmur 1: (Figure 3). Only the ranking of the Bam nesting site showed F4,15 = 10.02, p < 0.0001; Makmur 2: F4,15 = 7.20, p < 0.0001). a pronounced difference compared to Makmur 1. Its In Makmur 1, D. thoracicus colonies in Coc and Ban nests colonization rate (83.75%) was 23.75% higher than that at contained a significant higher number of larvae compared Makmur 1. In general, Coc was the artificial nesting site to Cac and Bag nests. Only Cac nest did not show a which proved to be most attractive for black cacao ants in significant difference compared to any other type of both studied cacao plantations. artificial nesting sites. In Makmur 2, Coc nest had a significant higher number of ant larvae compared to Cac, Bam and Bag nests, but not Ban nest which did not differ Effect of Artificial Ant Nests on Colony Size from all other types of artificial nesting sites (Figure 6). The number of ant pupae in D. thoracicus colonies Number of ant workers differed significantly at both study differed significantly at both study sites between the sites between artificial ant nests colonized by D. thoracicus different types of placed artificial nesting sites (one-way (one-way ANOVA; Makmur 1: F = 17.07, p < 0.0001; 4,15 ANOVA; Makmur 1: F4,15 = 5.12, p < 0.0001; Makmur 2: F4,15

Makmur 2: F4,15 = 12.21, p < 0.0001). In Makmur 1, Coc and = 9.25, p < 0.0001). In the cacao plantation of Makmur 1, Ban nests were occupied by significantly larger colonies Coc nests contained a significant higher number of pupae than other types of nesting sites (Cac, Bam, Bag). In Makmur than Bam and Bag nests. No significant differences were 2, only the mean number of workers in Coc nesting sites found between Ban and Cac nests and all other nests. At was significantly higher compared to other types of nesting Makmur 2 in Coc nests, significantly more pupae were sites (Figure 4). counted than that in all other nest types (Figure 7). For The number of ant queens differed significantly at both both cacao plantations, the comparison between cacao study sites between the artificial nesting sites colonized trees with and without artificial nesting sites (n = 20 trees by D. thoracicus (one-way ANOVA; Makmur 1: F4,15 = 8.77, per group) showed that trees with artificial nesting space 48 Meldy L.A. Hosang et al.

Makmur 1 Makmur 2 25000 25000 a 20000 20000 a a 15000 15000 b b 10000 10000 b b b 5000 5000 b b Number of ant workers Number of ant workers 0 0

-5000 -5000 Coc Ban Cac Bam Bag Coc Ban Cac Bam Bag

Artificial ant nest Artificial ant nest

Figure 4. Mean number of ant workers of Dolichoderus thoracicus per nest in different types of artificial nesting sites placed in cacao plantations of Makmur 1 and Makmur 2. Significant differences (Scheffé test) are marked by different letters. Coc = bundle of dry coconut leaflets, Ban = bundle of dry banana leaves, Cac = bundle of dry cacao leaves, Bam = bamboo filled with dry cacao leaves, and Bag = transparent plastic bag filled with dry cacao leaves.

Makmur 1 Makmur 2 200 200 a 150 150 a ab b 100 100 b b b b b 50 50

a 0 0 Number of ant queens Number of ant queens

-50 -50 Coc Ban Cac Bam Bag Coc Ban Cac Bam Bag

Artificial ant nest Artificial ant nest

Figure 5. Mean number of Dolichoderus thoracicus queens per nest counted in different types of artificial nesting sites in the cacao plantations of Makmur 1 and Makmur 2. Significant differences (Scheffé test) are marked with different letters. Coc = bundle of dry coconut leaflets, Ban = bundle of dry banana leaves, Cac = bundle of dry cacao leaves, Bam = bamboo filled with dry cacao leaves, and Bag = transparent plastic bag filled with dry cacao leaves.

Makmur 1 Makmur 2 200 200 a

150 150 a ab b 100 100 b b b b b 50 50

a 0 0 Number of ant larvae Number of ant larvae

-50 -50 Coc Ban Cac Bam Bag Coc Ban Cac Bam Bag

Artificial ant nest Artificial ant nest

Figure 6. Mean number of ant larvae in Dolichoderus thoracicus colonies in different types of artificial nesting sites in cacao plantations of Makmur 1 and Makmur 2. Significant differences (Scheffé test) are marked with different letters. Coc = bundle of dry coconut leaflets, Ban = bundle of dry banana leaves, Cac = bundle of dry cacao leaves, Bam = bamboo filled with dry cacao leaves, and Bag = transparent plastic bag filled with dry cacao leaves. The potential of artificial nesting sites ... 49

Makmur 1 Makmur 2

5000 5000 a 4000 ab 4000 ab 3000 3000 b 2000 b 2000 b 1000 b 1000 b b

Number of pupae 0 Number of pupae 0 a -1000 -1000

-2000 -2000 Coc Ban Cac Bam Bag Coc Ban Cac Bam Bag

Artificial ant nest Artificial ant nest

Figure 7. Mean number of ant pupae counted in Dolichoderus thoracicus colonies from different types of artificial nesting sites in cacao plantations of Makmur 1 and Makmur 2. Significant differences (Scheffé test) are marked with different letters. Coc = bundle of dry coconut leaflets, Ban = bundle of dry banana leaves, Cac = bundle of dry cacao leaves, Bam = bamboo filled with dry cacao leaves, and Bag = transparent plastic bag filled with dry cacao leaves.

had a significantly higher number of ants foraging on tree 900 Makmur 1 Makmur 2 trunks as well as on branches and leaves in the lower 700 t = 2.28 t = 3.73 canopy (Figure 8). df = 38 df = 38 The results showed that the black cacao ant D. 500 N = 20 N = 20 p = 0.028 p < 0.001 thoracicus was capable of establishing colonies in all of 300 five different artificial nesting sites placed in the cacao 100 trees, i.e. bundles of coconut leaves (Coc), of banana leaves Number of ants (Ban), of cacao leaves (Cac), hollow bamboo filled with -100 dry cacao leaves (Bam), and transparent plastic bags filled with cacao leaves (Bag). These colonies were not only -300 ‘satellite colonies´ but also reproductive colonies by YES NO YES NO themselves. This was confirmed by their large number of Artificial nesting site larvae and pupae. Most of the placed nesting sites were Figure 8. Mean number of counted/estimated Dolichoderus already colonized after 2 weeks. Therefore, it seems that thoracicus workers foraging in cacao trees nesting space is a major limiting factor for the density of D. (plantations Makmur 1 and Makmur 2) with (YES) and thoracicus in cacao plantations. without (NO) artificial nesting sites; N = number of When it comes to which type of artificial nesting sites observed pairs of cacao trees. can be recommended to farmers who intend to increase the density of black cacao ants in their plantations, the ranking of artificial nesting sites is Coc > Ban > Cac = Bam crowns of coconut palms, even those are more than 18 m = Bag. Dry coconut leaves (such as Ban and Cac) which tall. A variety of homopterans, including Cataenococcus are the cheapest way of providing additional nesting space hispidus (Morrison), reside on the leaves and fruits of the for D. thoracicus were already found to be perfect as coconut palms and black cacao ants attend them for their nesting space by Khoo (2001). He argued that the coconut honeydew, a source of sustenance (Khoo 2001). Honeydew palm was an excellent source of shelter for the black cacao from the mealy bug C. hispidus is the main source of food ants because aggregations of D. thoracicus could also for the black cacao ants although there are additional other naturally be found under coconut fronds. When the frond sources (Khoo and Chung 1989). Ho and Khoo (1997) becomes old and drops from the palm, the drying leaflets documented D. thoracicus using C. hispidus alone as a form long tubes, offering nesting site. source of food over an 8-week period of observation Cacao is commonly grown under shade trees such as without showing ill effects. A successful introduction of Gliricidia, Leucaena, Albizia and coconut. Of these shade the black cacao ants does not only depend on the type of trees, coconut palms were clearly favored by the black artificial nesting sites but also on the available food source cacao ants. Where the ant is well established, active trail and other factors such as the presence of other dominant can be seen running between the cacao trees and the ant species. 50 Meldy L.A. Hosang et al.

CONCLUSION REFERENCES

All types of artificial nesting sites were capable of Flint, M.L. and R. van den Bosch. 1981. Introduction to Integrated increasing the density of D. thoracicus in cacao plantations Pest Management. Plenum Press, New York. Giesberger, G. 1983. Biological control of Helopeltis of cocoa in and can be used to introduce black cacao ants in new Java. p. 91-180. In H. Toxopeus and P.C. Wessel. Cocoa locations. However, we recommend particularly nesting Research in Indonesia 1900-1950. American Cocoa Research sites prepared by using dry leaflets of coconut and banana Institute, International Office of Cocoa and Chocolate, leaves because they proved to be most successful in Wageningen. attracting D. thoracicus. Additionally, they are much Ho, C.T. and K.C. Khoo. 1997. Partners in biological control of cocoa pest: Mutualism between Dolichoderus thoracicus cheaper than nesting sites prepared by using bamboo or (Hymenoptera: Formicidae) and Cataenococcus hispidus plastic bags (filled with dry cacao leaves). Increasing the (Hemiptera: Pseudococcidae). Bull. Entomol. Res. 87: 461-470. population density of the black cacao ants in cacao trees Holldobler, B. and E.O. Wilson. 1990. The Ants. Springer-Verlag, may effectively contribute to the biological control of cacao Berlin. pests. Hosang, M.L.A. 2004. Interaction between Natural Enemies, Herbivores and Cacao in Palolo Valley, Central Sulawesi. PhD Dissertation, Graduate School Bogor Agricultural University. ACKNOWLEDGEMENTS Khoo, K.C. and G.F. Chung. 1989. Use of the black cacao ant to control mirid damage in cocoa. The Planter 65: 370-383. Khoo, K.C. and C.T. Ho. 1992. The influence of Dolichoderus Many thanks are extended to Prof. Dr. Sjafrida Manuwoto thoracicus (Hymenoptera: Formicidae) on losses due to and Dr. Purnama Hidayat (Bogor Agricultural University) Helopeltis theivora (Heteroptera: Miridae), black pod disease, for their support of the research, their valuable advice and and mammalian pests in cocoa in Malaysia. Bull. Entomol. many fruitful discussions. We are grateful to Prof. Dr. Res. 82: 485-491. Khoo, K.C. 2001. Controlling cocoa pests in Southeast Asia with Gerhard Gerold, Prof. Dr. Edi Guhardja, Dr. Andriyono Kilat the black cocoa ant. http://www.oardc.ohio-state.edu/cocoa/ Adhi, Diah Ratnadewi, Dr. Elim Somba, Dr. Silvia Werner, ants.htm. Widia Wati and Rina Yusuf of the German-Indonesian Perfecto, I. and A. Castineiras. 1998. Deployment of the Research Project STORMA and last but not least to all predaceous ants and their conservation in agroecosystems. p. STORMA drivers for their great support and help. 269-289. In P. Barbosa (Ed.). Conservation Biological Control. Furthermore, we thank to Pak Darman, Pak Edy and Haji Academic Press, San Diego. See, Y.A. and K.C. Khoo. 1996. Influence of Dolichoderus Saide, who assisted us in the field and gave permission to thoracicus (Hymenoptera : Formicidae) on cocoa pod damage conduct research on their land, Moh Iqbal, Iwan Suluk by Conopomorpha cramerella (Lepidoptera: Gracillariidae) Padang, Slamet Riadi, Rati Untari, Kent Kumajaya, Amar in Malaysia. Bull. Entomol. Res. 86: 467-474. Sakti and Ibar Mentauruk provided valuable help in the StatSoft. 1999. Statistica for Windows, 5.5. StatSoft Inc., Tulsa. field and assisted in sorting the samples. The research Way, M.J. and K.C. Khoo. 1989. Relationships between Helopeltis theobromae damage and ants with special reference to project was partly funded by the Deutsche Forschungs- Malaysian cocoa smallholdings. J. Plant Protection in the gemeinschaft (SFB 552). Tropics 6: 1-11.