ISSN 1411 – 0067 Jurnal Ilmu-Ilmu Pertanian Indonesia. Edisi Khusus, No. 3 2007, Hlm. 351 - 356 351

Odontoponera denticulata [:Formicidae]: A POTENTIAL BIOLOGICAL CONTROL AGENT FOR TRUE FRUIT FLIES [Diptera:Tephritidae] IN YOGYAKARTA, INDONESIA

Odontoponera denticulata [Hymenoptera:Formicidae] SEBAGAI AGENSIA PENGENDALI HAYATI LALAT BUAH [Diptera:Tephritidae] DI YOGYAKARTA, INDONESIA

Suputa1, Seiki Yamane2, Edhi Martono1, Zamir Hossain3, and Ahmad Taufiq Arminudin1 1Department of Plant Pests and Diseases, Faculty of Agriculture, Gadjah Mada University, Yogyakarta, Indonesia, [email protected] 2University of Kagoshima, Kyushu, Japan 3University of Western Sydney, Locked Bag 1797, Penrith South DC 1797, NSW, Australia

ABSTRACT

The number of active nest entrances under canopy, foraging distance, and the number of attacked true fruit flies larvae, predation ability, and the behavior of Odontoponera denticulata were observed in Yogyakarta, central part of Java. There are five dominant species of fruit trees grown in the home yards on Yogyakarta; mango (Mangifera indica), carambola (Averrhoa carambola), rose-apple (Syzygium aqueum), guava (Psidium guajava), rambutans (Nephelium lappaceum) and nut gnetum (Gnetum gnemon). We observed 100 sites at home yards randomly distributed in Yogyakarta city. The quantitative data were obtained by direct observation and the qualitative data e.g. the ’ behavior were obtained using digital photography and video camera techniques. The results show that the average number of active nest entrances under canopy was 9.36 + 1.59, foraging distance from the nest entrance was 113.34 + 57.98 (cm), number of attacked fruit fly larvae was 4.47 + 2.36, and predation ability (%) was 30.02 + 13.88. The ants attack active larvae only from fallen fruits; some ants did not attack nor notice the motionless larvae even as the ants stepped over the larvae, except when they already had experience in attacking larvae before. These conditions reveal that O. denticulata is more effective in attacking fruit fly larvae when they have former experience such as learning and memories and the existence of O. denticulata as a potential predator to reduce true fruit fly population at the home yards in Yogyakarta.

Key words: behavior, Odontoponera denticulata, predation, true fruit flies, Yogyakarta ABSTRAK

Pengamatan semut Odontoponera denticulata yang meliputi jumlah lubang sarang di bawah kanopi yang masih aktif, jarak jelajah pencarian pakan, kemampuan memangsa dan jumlah larva lalat buah yang diserang serta perilaku semut O. denticulata dilakukan di Yogyakarta. Ada lima spesies tumbuhan berbuah yang ditanam pada pekarangan rumah di Yogyakarta, yaitu: mangga (Mangifera indica), belimbing (Averrhoa carambola), jambu air (Syzygium aqueum), jambu biji (Psidium guajava), rambutan (Nephelium lappaceum) dan melinjo (Gnetum gnemon). Pengamatan dilakukan secara acak pada 100 pekarangan di kota Yogyakarta. Data kuantitatif diamati secara visual dan data kualitatif seperti perilaku semut diamati dengan menggunakan teknik kamera video dan kamera foto digital. Hasil penelitian menunjukkan bahwa rata-rata jumlah lubang sarang di bawah kanopi yang masih aktif adalah 9.36 + 1.59, jarak jelajah pencarian pakan dari lubang sarang adalah 113.34 + 57.98 (cm), jumlah larva lalat buah yang diserang adalah 4.47 + 2.36, dan kemampuan memangsa adalah 30.02 + 13.88 (%). Semut O. denticulata hanya memangsa larva lalat buah yang aktif pada buah jatuh; beberapa semut tidak menyerang larva lalat buah yang tidak bergerak bahkan ketika semut tersebut telah menginjaknya kecuali jika semut-semut tersebut telah mempunyai pengalaman menyerang larva lalat buah sebelumnya. Fenomena perilaku semut ini menggambarkan bahwa O. denticulata akan lebih efektif memangsa larva lalat buah ketika semut-semut tersebut mempunyai pengalaman memangsa larva lalat buah sebelumnya seperti pada proses pengingatan dan pembelajaran dan keberadaan O. denticulata di Yogyakarta terbukti sebagai predator potensial dalam menurunkan populasi lalat buah pada pekarangan di Yogyakarta.

Kata kunci: perilaku, Odontoponera denticulata, kemampuan memangsa, lalat buah, Yogyakarta Suputa et al., JIPI 352

INTRODUCTION please cite and mention here). Moreover, the role of Odontoponera denticulata in fruit fly Yogyakarta is located in the central part of predation has never been studied. A preliminary Java and lies within the tropics (latitude: 7° 48' study had found that the O. denticulata population South; longitude: 110° 30' East),. There are many in Yogyakarta was very high and can be found in species of fruit trees grown in the home yards almost every home yard (Suputa et al., 2005). such as mango (Mangifera indica), carambola The aim of this study was to determine the (Averrhoa carambola), rose-apple (Syzygium potential of O. denticulata as a predator of true aqueum), guava (Psidium guajava), rambutan fruit flies. The study examined their predation (Nephelium lappaceum), jackfruit (Artocarpus ability, their behavior including the number of active heterophylus), mahkota-dewa (Phaleria nest entrances under the tree canopy, the foraging macrocarpa), soursop (Annona muricata), pattern and the distance they travel to take true srikaya (Annona squamosa), breadfruit fruit fly larvae as a prey. (Artocarpus altilis), noni (Morinda citrifolia), citrus (Citrus sinensis), banana (Musa x MATERIALS AND METHODS paradisiaca), papaya (Carica papaya), sapodilla (Achras zapota), avocado (Persea americana), This study was carried out from June 2005 cashew (Anacardium occidentale), matoa to November 2005. We observed Odontoponera (Pometia pinnata), grapes (Vitis vinifera) and denticulata systematically on the soil surface gnetum (Gnetum gnemon). Many fruits cannot under fruits tree growing in the home yards in be harvested because of fruit fly infestation. The Yogyakarta on one hundred sites and collected most economically important true fruit fly individuals at each location manually using [Diptera: Tephritidae] species in Yogyakarta tweezers as voucher specimens. Collected belong to the Bactrocera spp. (Santianawati specimens, initially kept in small vials filled with et al. 1995). 80% ethanol, were taken to the Laboratory of the Insecticidal cover sprays have traditionally Basic Entomology to be dry-mounted on points been used to control fruit flies not only at the and labelled following the procedure of Hashimoto plantation but also at the home yard in Yogyakarta. and Rahman (2003). The voucher specimens are However, there are several disadvantages of kept in the collection at the Insect Museum insecticide cover sprays such as high cost, at the Department of Plant Protection, Faculty of difficulty in applying insecticide on dense Agriculture, Gadjah Mada University located in plantations, negative impact on insect natural Yogyakarta. enemies and also the possibility of harmful residues Direct behavioral observations were on fruits (Allwood, 1996; Putra, 2001). conducted randomly around mature fallen fruits Comparatively, biological control techniques are on the ground under the host plants. We recorded economical and environmentally friendly (Wilson the kind of fruit crop at every site and then and Huffaker, 1976). Most ants are predators; captured 100 samples of ant and marked them on which may play important roles in tropical their notum using a greenish yellow paint marker ecosystems which is a vital prerequisite for a (Yoka Paint Marker KP7-01) to identify biological control agent (Ogata, 1992). Fruit fly individuals. larvae are attacked by honey ants (genus We counted the number of attacked fruit fly Myrmecocystus) in Mexico (larvae of larvae, the numbers of remaining larvae in the Anastrepha ludens; Thomas, 1995) and by fallen rotten fruits, and the number of active Pheidole megacephala in Hawaii (larvae of entrances at every site. Ants foraging varies in Bactrocera dorsalis; Morgan, 1995). pattern (Figure 1 and 2). When the ants foraged Information about the natural enemies of true and did not find any kind of prey/food, they walked fruit flies in Yogyakarta is not available (if it is around in curved line and sometimes in circular Odontoponera denticulata JIPI 353 patterns, since they left the nest until their return. after taking a fruit fly larva, ant preferences on We chose these patterns to measure the distance true fruit flies larvae, and the foraging pattern of of ants foraging. We furthermore measured the O. denticulata. The recorded pictures were then foraging distance of ants under condition without transferred into hand drawings to illustrate the prey or any other kind of food since this might foraging pattern of O. denticulata. No insecticidal reflect the natural foraging distance. control of true fruit flies was done in the sampled We recorded ant activities with digital area, thus the results should reflect the natural photography and video camera techniques to status of O. denticulata as a predator of fruit fly observe the foraging behavior of ants before and larvae.

Figure 1. Foraging pattern O. denticulata: a) when the ants did not get a prey; b) when the ants got a prey

Figure 2. Foraging pattern O. denticulata, when the ants got a prey via difference active nest en- trance: a) got a prey on first time; b) got a prey on second time and more Suputa et al., JIPI 354

RESULTS AND DISCUSSION B. mcgregori. The most abundant species in 100 sites is B. carambolae i.e. 60% and then B. This research observed on 100 sites of the papayae i.e. 25% while B. albistrigata and B. home yard gardens habitat in Yogyakarta mcgregori respectively 10% and 5%. Drew and (Appendix Figure 1) and collected 100 specimens Hancock (1994) and Siwi et al. (2006) reported of Odontoponera spp. Kalshoven (1981) that these true fruit flies are serious pest in reported the more common O. transversa lives Indonesia and there was no appropriate method in the soil near houses in the middle area of Java to control these pests accurately yet. including Yogyakarta. The identification showed O. denticulata may function as a potential that all collected specimens of the ants genus true fruit flies predator as the population of O. Odontoponera belonged to O. denticulata. We denticulata at the home yards in Yogyakarta is presume that O. transversa mentioned in the very high and abundant (Suputa et al., 2005). study by Kalshoven (1981) might be O. Eguchi et al. (2004) state that O. denticulata denticulata, since their morphological characters colony was frequently found in Indo-chinese resemble those of O. denticulata. According to Lowland Vegetation. In the Bogor Botanical Bolton (1994) only one species in the genus Garden, the population of O. denticulata is higher Odontoponera is recognized and this view is widely than O. transversa (Ito et al., 2001). The average accepted. Seiki Yamane (personal communication, number of active nest entrance under canopy was October 11, 2005), however, identified two sibling 7.77 – 10.95 average is one number in this case species in this genus; i.e. O. transversa and O. 9.36 nest entrances with a minimum of 5 nest denticulata. entrances and a maximum of 12 nest entrances The O. denticulata population in Yogyakarta (Table 1). More nest entrances reflect more was very high and abundant with 9.36 + 1.59 active chance of true fruit fly larvae to be caught by the nest entrances in average (Suputa et al., 2005), ant. The potential of O. denticulate as predator the ants exist on every observation site in the home was not only shown by the number of active nest yard. There are also some other frequently entrance under canopy, but also by foraging encountered species in home yards but none of distance, number of attacking larvae, and predation them as abundant as O. denticulata. They are ability. Pheidole blutschlii, Oecophylla smaragdina, The average foraging distance of O. Solenopsis geminata, Diacamma denticulata was 113.34 + 57.98 cm with a pallidum, similis, Crematogaster minimum of in 40 cm and maximum of 350 cm sp., Polyrhachis bicolor, P. dives, Philidris sp., (Table 1). Eguchi et al. (2004) show that the Monomorium sp., and Dolichoderus sp. furthest foraging of O. denticulata in the For additional information, we also identified subtropical lowland vegetation was 116 cm. On the species of true fruit fly existed at the home the other hand, when the ants find prey/food, they yards habitat in Yogyakarta. We found Bactrocera walked straight from the target back to the nest carambolae, B. papayae, B. albistrigata, and entrance. Table 1. Number of Active Nest Entrances under Canopy (25 m2), Foraging Distance, Number of Attacked Larvae, and Predation Ability of Odontoponera denticulata in Yogyakarta home yards Variable Number of sample Average Min - Max Number of active nest entrance under canopy (25 m2) 100 sites 9.36 + 1.59 5 – 12 Foraging distance (cm) 100 ants 113.34 + 57.98 40 – 350 Number of attacked larvae 100 fruits 4.47 + 2.36 1 - 10 Predation ability (%) 100 fruits 30.02 + 13.88 6.66 - 90 Odontoponera denticulata JIPI 355

In observing feeding behavior, the first time [Kagawa University] for they motivated us to do forager, O. denticulata, showed more interest in this study and also provided us with research mobile than static larvae. Some forager ants did consultation. Independent research was program not attack nor notice the motionless larvae even of Basic Entomology Laboratory [Department of while the ants step over the larvae. As the second Plant Pests and Diseases, Faculty of Agriculture, time forager, O. denticulata is more aggressive Gadjah Mada University, Yogyakarta-Indonesia]. to catch both mobile or and static larvae, after they have already acquired experience in attacking REFERENCES larvae before. These phenomena indicate that former experience such as learning and memories Allwood, A.J. 1996. Control Strategies for Fruit are important for O. denticulata as a true fruit Flies (Family Tephritidae) in the South Pacific. fly predator. This is not unlikely since other social p. 171-178, in A.J. Allwood & R.A.I. Drew insect use learning and memories during foraging, (eds.). Management of Fruit Flies in the e.g. bees (Menzel et al., 1991). The average Pacific. ACIAR Proceedings No. 76. A number of attacked larvae was 4.47 + 2.36 larvae Regional Symposium. Nadi. Fiji. with a minimum of 1 larva and maximum of 10 Bolton, B. 1994. Identification Guide to the Ant larvae. The average of O. denticulata predation Genera of the World. Harvard University ability was 30.02 + 13.88% with a minimum of Press. Cambridge. Massachusetts. London, 6.66% and a maximum of 90%. O. denticulata England. as predators exhibited high population in the home Drew, R.A.I. and D.L. Hancock. 1994. The yards, and there was no host plant preferences Bactrocera dorsalis complex of fruit flies shown by the ants in attacking prey larvae on (Diptera: Tephritidae: Dacinae) in Asia. different plant species. Bulletin of Entomological Research. Supplement. 2:1-68 CONCLUSIONS Eguchi, K., T.V. Bui, and S. Yamane. 2004. A preliminary study on foraging distance and Generally the predation ability of O. nesting sites of ants in Indo-Chinese lowland denticulata belongs to low to medium level. vegetation (Insect, Hymenoptera, Former experiences such as learning and memories Formicidae). Sociobiology. 43(3): 445-457 are important in O. denticulata as a true fruit fly Hashimoto, Y., and H. Rahman. 2003. Inventory predator. The right methods must be found to and collection. Total protocol for establish synergistic association and to maximize understanding of . BBEC the role of O. denticulata as a predator in Publication No. 6. 310 p. controlling true fruit flies population in Yogyakarta. Ito, F., S. Yamane, K. Eguchi, W.A. Noerdjito, S. Kahono, K. Tsuji, K. Ohkawara, K. ACKNOWLEDGMENTS Yamauchi, T. Nishida, and K. Nakamura. 2001. Ant species diversity in the Bogor The authors are gratefully acknowlege Dr. Botanic Garden, West Java, Indonesia, with Joachim Offenberg [University of AArhus, descriptions of two new species of the genus Denmark], Dr. Steve Shattuck [CSIRO, Australia], Leptanilla (Hymenoptera, Formicidae). Dr. Ian Naumann [DAFF, Australia], Prof. Datin Tropics. 10(3): 379-404 Dr. Maryati Mohamed and Dr. Bakhtiar Effendi Kalshoven, L.G.E. 1981. The Pest of Crops in Yahya [Universiti Malaysia Sabah, Malaysia], Dr. Indonesia. P.T. Ichtiar Baru Van Hoeve. Katsuyuki EGUCHI [Kagoshima University], Dr. Jakarta, Indonesia. Yoshiaki HASHIMOTO [Hyogo Prefectural Menzel, R., M. Hammer, G. Braun, J. University], Dr. Nugroho Susetya Putra [Gadjah Mauelshagen, and M. Sugawa. 1991. Mada University, Indonesia], and Fuminori ITO Neurobiology of learning and memory in Suputa et al., JIPI 356

honeybees. p. 323-353, in Goodman, L.J. The Revisi. Diterbitkan oleh Balai Besar Behaviour and Physiology of Bees. C.A.B. Penelitian dan Pengembangan Bioteknologi International. dan Sumberdaya Genetik Pertanian Morgan, R.C. 1995. Honey i swelled the kids: Indonesia dan Department of Agriculture, ambitious ants store liquid food for dry times. Fisheries and Forestry Australia. http://www.sasionline.org/antsfiles/pages/ Suputa, O.D. Raharjo, dan A. Taufiq. 2005. Native honeyants/honey.html. Originally published natural enemies of true fruit flies (Diptera: in Backyard BUGWatching #16, 1995. Tephritidae) in Yogyakarta. Scientific Poster. Ogata, K. 1992. The ant fauna of the oriental International Conference of Crops Security. region: an overview (Hymenoptera, Brawijaya University. Malang. East Java. Formicidae). Bulletin of the Institute of Indonesia. Tropical Agriculture. Kyushu University. 15: Thomas, D.B. 1995. Predation on the soil 55-74 inhabiting stages of the Mexican fruit fly. Putra, N.S. 2001. Hama Lalat Buah dan Southwestern Entomologist. 20(1): 61-71 Pengendaliannya. Penerbit Kanisius, Wilson, F. and C.B. Huffaker. 1976. The Yogyakarta. Philosophy, Scope, and Importance of Santianawati, B.A. Suripto, R.C.H. Soesilohadi, Biological Control. p. 3-15, in: Huffaker, C.B. dan Purnomo. 1995. Analisis Bactrocera spp. & P.S. Messenger. Theory and Practice of kompleks (Diptera: Tephritidae) di Daerah Biological Control. The International Istimewa Yogyakarta. P4M/DPPM Dirjen Organization for Biological Control and The Dikti-UGM. Siwi, S.S., P. Hidayat, dan Suputa. 2006. International Center for Biological Control. Taksonomi dan Bioekologi Lalat Buah Penting University of California. Academic Press, di Indonesia (Diptera: Tephritidae). Edisi INC, New York.