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ISSN 1411 – 0067 Jurnal Ilmu-Ilmu Pertanian Indonesia. Edisi Khusus, No. 3 2007, Hlm. 351 - 356 351 Odontoponera denticulata [Hymenoptera: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 1 Department of Plant Pests and Diseases, Faculty of Agriculture, Gadjah Mada University, Yogyakarta, Indonesia, [email protected] 2 University of Kagoshima, Kyushu, Japan 3 University 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 ants’ 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., INTRODUCTION Yogyakarta is located in the central part of Java and lies within the tropics (latitude: 7° 48' South; longitude: 110° 30' East),. There are many species of fruit trees grown in the home yards such as mango (Mangifera indica), carambola (Averrhoa carambola), rose-apple (Syzygium aqueum), guava (Psidium guajava), rambutan (Nephelium lappaceum), jackfruit (Artocarpus heterophylus), mahkota-dewa (Phaleria macrocarpa), soursop (Annona muricata), srikaya (Annona squamosa), breadfruit (Artocarpus altilis), noni (Morinda citrifolia), citrus (Citrus sinensis), banana (Musa x paradisiaca), papaya (Carica papaya), sapodilla (Achras zapota), avocado (Persea americana), cashew (Anacardium occidentale), matoa (Pometia pinnata), grapes (Vitis vinifera) and gnetum (Gnetum gnemon). Many fruits cannot be harvested because of fruit fly infestation. The most economically important true fruit fly [Diptera: Tephritidae] species in Yogyakarta belong to the genus Bactrocera spp. (Santianawati et al. 1995). Insecticidal cover sprays have traditionally been used to control fruit flies not only at the plantation but also at the home yard in Yogyakarta. However, there are several disadvantages of insecticide cover sprays such as high cost, difficulty in applying insecticide on dense plantations, negative impact on insect natural enemies and also the possibility of harmful residues on fruits (Allwood, 1996; Putra, 2001). Comparatively, biological control techniques are economical and environmentally friendly (Wilson and Huffaker, 1976). Most ants are predators; which may play important roles in tropical ecosystems which is a vital prerequisite for a biological control agent (Ogata, 1992). Fruit fly larvae are attacked by honey ants (genus Myrmecocystus) in Mexico (larvae of Anastrepha ludens; Thomas, 1995) and by Pheidole megacephala in Hawaii (larvae of Bactrocera dorsalis; Morgan, 1995). Information about the natural enemies of true fruit flies in Yogyakarta is not available (if it is JIPI 352 please cite and mention here). Moreover, the role of Odontoponera denticulata in fruit fly predation has never been studied. A preliminary study had found that the O. denticulata population in Yogyakarta was very high and can be found in almost every home yard (Suputa et al., 2005). The aim of this study was to determine the potential of O. denticulata as a predator of true fruit flies. The study examined their predation ability, their behavior including the number of active nest entrances under the tree canopy, the foraging pattern and the distance they travel to take true fruit fly larvae as a prey. MATERIALS AND METHODS This study was carried out from June 2005 to November 2005. We observed Odontoponera denticulata systematically on the soil surface under fruits tree growing in the home yards in Yogyakarta on one hundred sites and collected ant individuals at each location manually using tweezers as voucher specimens. Collected specimens, initially kept in small vials filled with 80% ethanol, were taken to the Laboratory of the Basic Entomology to be dry-mounted on points and labelled following the procedure of Hashimoto and Rahman (2003). The voucher specimens are kept in the insect collection at the Insect Museum at the Department of Plant Protection, Faculty of Agriculture, Gadjah Mada University located in Yogyakarta. Direct behavioral observations were conducted randomly around mature fallen fruits on the ground under the host plants. We recorded the kind of fruit crop at every site and then captured 100 samples of ant and marked them on their notum using a greenish yellow paint marker (Yoka Paint Marker KP7-01) to identify individuals. We counted the number of attacked fruit fly larvae, the numbers of remaining larvae in the fallen rotten fruits, and the number of active entrances at every site. Ants foraging varies in pattern (Figure 1 and 2). When the ants foraged and did not find any kind of prey/food, they walked around in curved line and sometimes in circular Odontoponera denticulata patterns, since they left the nest until their return. We chose these patterns to measure the distance of ants foraging. We furthermore measured the foraging distance of ants under condition without prey or any other kind of food since this might reflect the natural foraging distance. We recorded ant activities with digital photography and video camera techniques to observe the foraging behavior of ants before and JIPI 353 after taking a fruit fly larva, ant preferences on true fruit flies larvae, and the foraging pattern of O. denticulata. The recorded pictures were then transferred into hand drawings to illustrate the foraging pattern of O. denticulata. No insecticidal control of true fruit flies was done in the sampled area, thus the results should reflect the natural status of O. denticulata as a predator of fruit fly 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 entrance: a) got a prey on first time; b) got a prey on second time and more Suputa et al., RESULTS AND DISCUSSION This research observed on 100 sites of the home yard gardens habitat in Yogyakarta (Appendix Figure 1) and collected 100 specimens of Odontoponera spp. Kalshoven (1981) reported the more common O. transversa lives in the soil near houses in the middle area of Java including Yogyakarta. The identification showed that all collected specimens of the ants genus Odontoponera belonged to O. denticulata. We presume that O. transversa mentioned in the study by Kalshoven (1981) might be O. denticulata, since their morphological characters resemble those of O. denticulata. According to Bolton (1994) only one species in the genus Odontoponera is recognized and this view is widely accepted. Seiki Yamane (personal communication, October 11, 2005), however, identified two sibling species in this genus; i.e. O. transversa and O. denticulata. The O. denticulata population in Yogyakarta was very high and abundant with 9.36 + 1.59 active nest entrances in average (Suputa et al., 2005), the ants exist on every observation site in the home yard. There are also some other frequently encountered species in home yards but none of them as abundant as O. denticulata. They are Pheidole blutschlii, Oecophylla smaragdina, Solenopsis geminata, Diacamma pallidum,Odontomachus similis, Crematogaster sp., Polyrhachis bicolor, P. dives, Philidris sp., Monomorium sp., and Dolichoderus sp. For additional information, we also identified the species of true fruit fly existed at the home yards habitat in Yogyakarta. We found Bactrocera carambolae, B. papayae, B. albistrigata, and JIPI 354 B. mcgregori. The most abundant species in 100 sites is B. carambolae i.e. 60% and then B. papayae i.e. 25% while B. albistrigata and B. mcgregori respectively 10% and 5%. Drew and Hancock (1994) and Siwi et al. (2006) reported that these true fruit flies are serious pest in Indonesia and there was no appropriate method to control these pests accurately yet. O. denticulata may function as a potential true fruit flies predator as the population of O. denticulata at the home yards in Yogyakarta is very high and abundant (Suputa et al., 2005). Eguchi et al. (2004) state that O. denticulata colony was frequently found in Indo-chinese Lowland Vegetation. In the Bogor Botanical Garden, the population of O. denticulata is higher than O. transversa (Ito et al., 2001). The average number of active nest entrance under canopy was 7.77 – 10.95 average is one number in this case 9.36 nest entrances with a minimum of 5 nest entrances and a maximum of 12 nest entrances (Table 1). More nest entrances reflect more chance of true fruit fly larvae to be caught by the ant. The potential of O. denticulate as predator was not only shown by the number of active nest entrance under canopy, but also by foraging distance, number of attacking larvae, and predation ability. The average foraging distance of O. denticulata was 113.34 + 57.98 cm with a minimum of in 40 cm and maximum of 350 cm (Table 1). Eguchi et al. (2004) show that the furthest foraging of O. denticulata in the subtropical lowland vegetation was 116 cm. On the other hand, when the ants find prey/food, they walked straight from the target back to the nest 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 In observing feeding behavior, the first time forager, O. denticulata, showed more interest in mobile than static larvae. Some forager ants did not attack nor notice the motionless larvae even while the ants step over the larvae. As the second time forager, O. denticulata is more aggressive to catch both mobile or and static larvae, after they have already acquired experience in attacking larvae before. These phenomena indicate that former experience such as learning and memories are important for O. denticulata as a true fruit fly predator. This is not unlikely since other social insect use learning and memories during foraging, e.g. bees (Menzel et al., 1991). The average number of attacked larvae was 4.47 + 2.36 larvae with a minimum of 1 larva and maximum of 10 larvae. The average of O. denticulata predation ability was 30.02 + 13.88% with a minimum of 6.66% and a maximum of 90%. O. denticulata as predators exhibited high population in the home yards, and there was no host plant preferences shown by the ants in attacking prey larvae on different plant species. CONCLUSIONS Generally the predation ability of O. denticulata belongs to low to medium level. Former experiences such as learning and memories are important in O. denticulata as a true fruit fly predator. The right methods must be found to establish synergistic association and to maximize the role of O. denticulata as a predator in controlling true fruit flies population in Yogyakarta. ACKNOWLEDGMENTS The authors are gratefully acknowlege Dr. Joachim Offenberg [University of AArhus, Denmark], Dr. Steve Shattuck [CSIRO, Australia], Dr. Ian Naumann [DAFF, Australia], Prof. Datin Dr. Maryati Mohamed and Dr. Bakhtiar Effendi Yahya [Universiti Malaysia Sabah, Malaysia], Dr. Katsuyuki EGUCHI [Kagoshima University], Dr. Yoshiaki HASHIMOTO [Hyogo Prefectural University], Dr. Nugroho Susetya Putra [Gadjah Mada University, Indonesia], and Fuminori ITO JIPI 355 [Kagawa University] for they motivated us to do this study and also provided us with research consultation. 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