Drone-assisted augmentation of the parasitoid Anagyrus lopezi for cassava mealybug control in Indonesia

Main Article Content

MUHAMMAD ALIMUN WASIK
DEWI SARTIAMI
ALI NURMANSYAH

Abstract

Abstract. Wasik MA, Sartiami D, Nurmansyah A. 2025. Drone-assisted augmentation of the parasitoid Anagyrus lopezi for cassava mealybug control in Indonesia. Biodiversitas 26: 6437-6446. The cassava mealybug, Phenacoccus manihoti, is an invasive pest that causes severe damage and economic loss in cassava production in Indonesia. Biological control using the parasitoid Anagyrus lopezi to manage P. manihoti has proven effective; however, its manual releases remain constrained by time, labor, and cost. This study evaluated the effectiveness and operational efficiency of A. lopezi augmentation using drone-assisted and manual release techniques in cassava fields. Effectiveness was measured by the parasitism rate of A. lopezi on P. manihoti, while efficiency was assessed through cost and time analyses. The augmentation treatment significantly increased the parasitism rate (F = 1955.78; df = 2,11; p<0.001). Parasitism rates under both release techniques were 47.18±0.92% for drones and 46.87±1.04% for manual release, compared with 16.11±0.59% in the control plots. The comparable parasitism rates achieved by drone-assisted and manual releases indicate that drone deployment maintains comparable biological effectiveness to manual augmentation. Moreover, drone application requires only 25 minutes per hectare, compared to 200 minutes per hectare manually. Although the initial cost of drone use was higher at small operational scales, economic analysis indicated a break-even point at approximately 25 ha. These findings demonstrate the feasibility of drone-assisted parasitoid deployment as an operationally efficient approach for large-scale biological control of P. manihoti. This contribution strengthens area-wide Integrated Pest Management (IPM) programs by enabling synchronized parasitoid augmentation while also supporting the broader development of smart-agriculture technologies for cassava-based farming systems.

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Author Biographies

DEWI SARTIAMI, Department of Plant Protection, Faculty of Agriculture, Institut Pertanian Bogor. Jl. Kamper IPB Dramaga Campus, Bogor 16680, West Java, Indonesia

Dr. Dra. Dewi Sartiami, M.Si. is a lecturer at the Department of Plant Protection, Faculty of Agriculture, IPB University, Indonesia. Her research interests include insect taxonomy, entomology, and the biological control of agricultural pests.

ALI NURMANSYAH, Department of Plant Protection, Faculty of Agriculture, Institut Pertanian Bogor. Jl. Kamper IPB Dramaga Campus, Bogor 16680, West Java, Indonesia

Dr. Ir. Ali Nurmansyah, M.Si. is a lecturer at the Department of Plant Protection, Faculty of Agriculture, IPB University, Indonesia. His expertise includes statistics, forecasting of pest populations, and integrated pest management.

References

Abduchalek B, Rauf A, Pudjianto. 2017. Kutu putih singkong, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae): Persebaran geografi di Pulau Jawa dan rintisan pengendalian hayati. Jurnal Hama dan Penyakit Tumbuhan Tropika 17: 1-8. DOI: 10.23960/j.hptt.1171-8. [Indonesian]

Adriani E, Rauf A, Pudjianto. 2020. Influence of host stage on oviposition, development, and sex ratio of Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae), a parasitoid of the cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). Jurnal Hama dan Penyakit Tumbuhan Tropika 20: 130-139. DOI: 10.23960/jhptt.220130-139.

Agrawal J, Arafat MY. 2024. Transforming farming: A review of AI-powered UAV technologies in precision agriculture. Drones 8 (11): 664-689. DOI: 10.3390/drones8110664.

Baoua IB, Ba MN, Amadou L, Kabore A, Dabire-Binso CL. 2018. Field dispersal of the parasitoid wasp Habrobracon hebetor (Hymenoptera: Braconidae) following augmentative release against the millet head miner Heliocheilus albipunctella (Lepidoptera: Noctuidae) in the Sahel. Biocontrol Sci Technol 28 (4): 404-415. DOI: 10.1080/09583157.2018.1450842.

Borase DN, Thorat YE, Baitha A, Kolkar BE. 2024. Parasitizing efficiency of Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae) on Galleria mellonella (Linnaeus) (Lepidoptera: Pyralidae) larva and pupa. Egypt J Biol Pest Control 34: 14. DOI: 10.1186/s41938-024-00777-5.

Burgio G, Magagnoli S, Mondini R, Guerrieri E, Casoli L, Profeta M, Capponcelli S, Castiglioni A, Meglioraldi S, Mora M, Valeriani S, Parrilli M. 2025. Area-wide augmentation of Anagyrus vladimiri and Cryptolaemus montrouzieri enhances biological control of mealybugs in Lambrusco vineyards in Northern Italy. Biol Control 206: 105800. DOI: 10.1016/j.biocontrol.2025.105800.

Cluever JD, Beiermann CW, Lawrence NC, Bradshaw JD. 2023. Assessing the toxicity of selected pesticides to Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) pupae as a first step in developing a potential novel deployment programme. Biocontrol Sci Technol 33 (11): 1065-1084. DOI: 10.1080/09583157.2023.2275116.

Dionne A, Khelifi M, Todorova S, Boivin G. 2018. Design and testing of a boom sprayer prototype for release of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in sweet corn for biocontrol of Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae). Transactions ASABE 61 (6): 1867-1879. DOI: 10.13031/trans.12922.

Fanani MZ, Rauf A, Maryana N, Nurmansyah A, Hindayana D. 2019. Geographic distribution of the invasive mealybug Phenacoccus manihoti and its introduced parasitoid Anagyrus lopezi in parts of Indonesia. Biodiversitas 20: 3751-3757. DOI: 10.13057/biodiv/d201238.

Fanani MZ, Rauf A, Maryana N, Nurmansyah A, Hindayana D. 2020. Parasitism of cassava mealybug by Anagyrus lopezi: Effects of varying host and parasitoid densities. Biodiversitas 21 (10): 4973-4980. DOI: 10.13057/biodiv/d211064.

Filho FHI, Heldens WB, Kong Z, de Lange ES. 2020. Drones: Innovative technology for use in precision pest management. J Econ Entomol 113 (1): 1-25. DOI: 10.1093/jee/toz268.

Guebsi R, Mami S, Chokmani K. 2024. Drones in precision agriculture: A comprehensive review of applications, technologies, and challenges. Drones 8 (11): 686-716. DOI: 10.3390/drones8110686.

Gundreddy RR, Alekhya G, Madhuri V, Jayanth BV, Darjee S, Shashikala MB, Reddy T, Gaddam NR. 2024. Actuation drones in agriculture: Advancing precision pest management through biocontrol and modern techniques. J Exp Agric Intl 46 (9): 825-35. DOI: 10.9734/jeai/2024/v46i92879.

Hwang JS, Kim WS. 2025. Evaluation of the field performance and economic feasibility of mechanized onion production in Korea. Agronomy 15: 1721. DOI: 10.3390/agronomy15071721.

Joshi S, Pai SG, Deepthy KB, Ballal CR, Watson GW. 2020. The cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Coccomorpha: Pseudococcidae) arrives in India. Zootaxa 4772 (1): 191-194. DOI: 10.11646/zootaxa.4772.1.8.

Junior JCA, Nunez DNC. 2023. The use of drones in agriculture 4.0. Braz J Sci 3 (1): 1-13. DOI: 10.14295/bjs.v3i1.438.

Kim J, Huebner CD, Reardon R, Park YL. 2021. Spatially targeted biological control of mile-a-minute weed using Rhinoncomimus latipes (Coleoptera: Curculionidae) and an unmanned aircraft system. J Econ Entomol 114 (5): 1889-1895. DOI: 10.1093/jee/toab020.

Lake EC, David AS, Spencer TM, Wilhelm VL, Barnett TW, Abdel-Kader AA, Cortes AC, Acuna A, Mattison ED, Minteer CR. 2020. First drone releases of the biological control agent Neomusotima conspurcatalis on old world climbing fern. Biocontrol Sci Technol 31 (1): 97-106. DOI: 10.1080/09583157.2020.1828280.

Lema KM, Herren HR. 1985. Release and establishment in Nigeria of Epidinocarsis lopezi a parasitoid of the cassava mealybug, Phenacoccus manihoti. Entomol Exp Appl 38: 171-175. DOI: 10.1111/j.1570-7458.1985.tb03515.x.

Lubis MAF, Wirianata H, Wilisiani F. 2024. Perbandingan pengendalian Curvularia sp. dengan drone dan manual pada pembibitan main nursery. Agroforetech 3 (2): 1163-1169. [Indonesian]

Mahhendra DW, Mawandha HG, Yuniasih B. 2025. Perbandingan teknis penyemprotan gulma secara manual dan menggunakan drone sprayer di lahan replanting. Agroista 8: 120-127. DOI: 10.55180/agi.v8i2.851. [Indonesian]

Mani M, Shivaraju C. 2016. Mealybugs and Their Management in Agricultural and Horticultural Crops. Springer, India.

Marina CF, Liedo P, Bond JG, Osorio AR, Valle J, Angulo-Kladt R, Gomez-Simuta Y, Fernandez-Salas I, Dor A, Williams T. 2022. Comparison of ground release and drone-mediated aerial release of Aedes aegypti sterile males in Southern Mexico: Efficacy and challenges. Insects 13: 347. DOI: 10.3390/insects13040347.

Martel V, Johns R, Tanguay LJ, Jean F, Maltais A, Trudeau S, St-Onge M, Cormier D, Smith SM, Boisclair J. 2021. The use of UAV to release the egg parasitoid Trichogramma spp. (Hymenoptera: Trichogrammatidae) against an agricultural and a forest pest in Canada. J Econ Entomol 14: 1867-1881. DOI: 10.1093/jee/toaa325.

Moretti E, Schmidt-Jeffris RA. 2025. Evaluation of drone and ground releases of Cryptolaemus montrouzieri for mealybug (Pseudococcus maritimus) control in apples. Biol Control 207: 105805. DOI: 10.1016/j.biocontrol.2025.105805.

Moses-Gonzales N, Adams CG, Conway H, Krompetz D, Rodriguez R, Baez I, Milam M. 2021. The use of multiple unmanned aircraft systems as a swarm to release sterile Mexican fruit fly (Diptera: Tephritidae) into South Texas citrus groves. J Econ Entomol 114 (5): 1857-1866. DOI: 10.1093/jee/toab024.

Mourya PK, Singh JK, Chaudhary P, Chaudhary AK, Upadhayay V. 2024. Role of drone technology in insect pest management. Vigyan Varta 5 (2): 104-107.

Muniappan R, Shepard BM, Watson GW, Carner GR, Rauf A, Sartiami D, Hidayat P, Afun JVK, Goergen G, Rahman AKMZ. 2011. New records of invasive insects (Hemiptera: Sternorrhyncha) in Southern Asia and West Africa. J Asia-Pac Entomol 26 (4): 167-174. DOI: 10.3954/1523-5475-26.4.167.

Naharki K, Hayes C, Park YL. 2024. Aerial systems for releasing natural enemy insects of purple loosestrife using drones. Drones 8 (11): 635-650. DOI: 10.3390/drones8110635.

Naimah F, Sartiami D, Maryana N, Anwar R, Pudjianto. 2023. Parasitoid of cassava mealybug, Anagyrus lopezi (Hymenoptera: Encyrtidae): mummy size, adult emergence, sex ratio, and parasitization level. Biodiversitas 24 (3): 1629-1634. DOI: 10.13057/biodiv/d240335.

Nopriawansyah N, Rauf A, Kusumah YM, Nurmansyah A, Koesmaryono Y. 2019. Genetic variation among the geographic population of cassava mealybug, Phenacoccus manihoti (Hemiptera: Pseudococcidae), in Indonesia inferred from mitochondrial COI gene sequence. Biodiversitas 20 (9): 1685-1692. DOI: 10.13057/biodiv/d200933.

Parsa S, Kondo T, Winotai A. 2012. The cassava mealybug (Phenacoccus manihoti) in Asia: First records, potential distribution, and an identification key. PLoS One 10 (7): e0047675. DOI: 10.1371/journal.pone.0047675.

Pozo-Valdivia AID, Morgan E, Bennett C. 2021. In-field evaluation of drone released lacewings for aphid control in California organic lettuce. J Econ Entomol 114: 1882-1888. DOI: 10.1093/jee/toab125.

Pu’u YMSW. 2019. Relationship between population and intensity of cassava mealybug (Phenacoccus manihoti) attack on Flores Island. J Sustain Agric 34 (1): 61-66. DOI: 10.20961/carakatani.v34i1.25974.

Salazar-Mendoza P, Rodríguez-Saona C, Fernandes OA. 2020. Release density, dispersal capacity, and optimal rearing conditions for Telenomus remus, an egg parasitoid of Spodoptera frugiperda, in maize. Biocontrol Sci Technol 30 (10): 1040-1059. DOI: 10.1080/09583157.2020.1776841.

Salerno G, Rebora M, Piersanti S, Gorb E, Gorb S. 2024. Parasitoid attachment ability and the host surface wettability. Zoology 165: 126181. DOI: 10.1016/j.zool.2024.126181.

Sandanayaka WRM, Charlesa JG, Davisa VA, Chhagana A, Shawb PW, Colec LM, Colhound K, Wallis DR. 2018. Mass rearing and release of Mastrus ridens (Hym: Ichneumonidae) a parasitoid for the biological control of codling moth Cydia pomonella. N Z Entomol 41 (2): 37-45. DOI: 10.1080/00779962.2018.1533067.

Sartiami D, Watson GW, Roff M, Hanifah MD, Idris AB. 2015. First record of cassava mealybug, Phenacoccus manihoti (Hemiptera: Pseudococcidae), in Malaysia. Zootaxa 3957 (2): 235-238. DOI: 10.11646/zootaxa.3957.2.8.

Sigsgaard L, Herz A, Korsgaard M, Wuhrer B. 2017. Mass release of Trichogramma evanescens and T. cacoeciae can reduce damage by the apple codling moth Cydia pomonella in organic orchards under pheromone disruption. Insects 8: 41. DOI: 10.3390/insects8020041.

Song C, Wang Q, Wang G, Liu L, Zhang T, Han J, Lan Y. 2023. Study on the design and experiment of Trichogramma ball delivery system based on agricultural drone. Drones 7 (10): 632-649. DOI: 10.3390/drones7100632.

Supartha IW, Widaningsih D, Susila IW, Yudha IKW, Utama IWEK, Wiradana PA. 2022. Range of host plants, spatial distribution, and insect predator of Phenacoccus manihoti (Hemiptera: Pseudococcidae) as an emerging pest of cassava plants in Bali, Indonesia. Biodiversitas 23 (6): 3022-3030. DOI: 10.13057/biodiv/d230629.

Supartha IW, Yudha IKW, Wiradana PA, Susila IW. 2020. Response of parasitoids to invasive pest Phenacoccus manihoti Matile Ferrero (Hemiptera: Pseudococcidae) on cassava crop in Bali, Indonesia. Biodiversitas 21 (10): 4543-4549. DOI: 10.13057/biodiv/d211011.

Suvittawat A. 2024. Investigating farmers’ perceptions of drone technology in Thailand: Exploring expectations, product quality, perceived value, and adoption in agriculture. Agriculture 14 (12): 2183-2208. DOI: 10.3390/agriculture14122183.

Syarief M, Rahmawati D, Mujiono, Fittryah LD. 2024. Effectiveness and efficiency of drone sprayer for weed control in rice (Oryza sativa L). Agriprima 8 (1): 52-60. DOI: 10.25047/agriprima.v8i1.523.

Thancharoen A, Lankaew S, Moonjuntha P, Wongphanuwat T, Sangtongpraow B, Ngoenklan R, Kittipadakul P, Wyckhuys KAG. 2018. Effective biological control of an invasive mealybug pest enhances root yield in cassava. J Pest Sci 91 (10): 1199-1211. DOI: 10.1007/s10340-018-1012-y.

Umeda S, Yoshikawa N, Seo Y. 2022. Cost and workload assessment of agricultural drone sprayer: A case study of rice production in Japan. Sustainability 17 (14): 10850. DOI: 10.3390/su141710850.

Wang S, Libo W, Jiawen L, Dayu Z, Tongxian L. 2021. Multiple mating of Aphelinus asychis enhance the number of female progeny but shorten the longevity. Insects 12 (9): 823. DOI: 10.3390/insects12090823.

Wasik MA, Sartiami D, Nurmansyah A. 2025. Mass production model of the parasitoid Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae) using the mealybug Phenacoccus manihoti Matile-Ferrero in the laboratory. Indones J Entomol 22: 114-125. DOI: 10.5994/jei.22.1.114.

Winotai A, Goergen G, Tamo M, Neuenchwander P. 2010. Cassava mealybug has reached Asia. Biocontrol News Inf 31: 10N-11N.

Wyckhuys KAG, Rauf A, Ketelaar J. 2014. Parasitoid introduced into Indonesia: Part of a region-wide campaign to tackle emerging cassava pests and diseases. Biocontrol News Inf 35 (4): 35-37.

Xia S, Ma N, Wang P, Lu Y. 2025. Effects of temperature and humidity on the fitness of aphid parasitoid, Binodoxys communis. Insects 16 (3): 264. DOI: 10.3390/insects16030264.

Yonow T, Kriticos DJ, Ota N. 2017. The potential distribution of cassava mealybug (Phenacoccus manihoti), a threat to food security for the poor. PLoS One 12: e0173265. DOI: 10.1371/journal.pone.0173265.

Yuan X, Guo Y, Li D. 2024. Field control effect of Telenomus remus Nixon and Trichogramma chilonis Ishii compound parasitoid balls against Spodoptera frugiperda (J. E. Smith). Insects 15 (1): 28. DOI: 10.3390/insects15010028.

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