Response of parasitoids to invasive pest Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) on cassava crop in Bali, Indonesia




Abstract. 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: 4543-4549. Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) is an invasive pest that entered Indonesia in 2010 and attacks cassava plants, especially in Bali Province. This study aimed to identify species and establish the population distribution mapping, community structures (diversity, abundance, and dominance), and parasitization rate on cassava crops in Bali. This study conducted with a field observation method by taking infested shoots of cassava plants by P. manihoti purposively in the field. The cassava mealybug that was present in the leaves or shoots were kept in the laboratory until the parasitoid appeared. The results showed that four species of parasitoids were found to respond to invasive pest, namely Anagyrus lopezi (Encyrtidae), Acerophagus sp. (Encyrtidae), Blepyrus sp. (Encyrtidae) and Encarsia sp. (Aphelinidae). Structurally the parasitoid community had a low abundance (R1 = 0.50–0.87) and low diversity index value (H'= 0.27-0.28). While the parasitoid dominance index was in the moderate category with a value D = 0.33–0.59 in Bangli, Klungkung, Badung, Tabanan, and Buleleng Districts. But it had high dominance index values in Gianyar, Denpasar, Jembrana, and Karangasem Districts with a value D = 0.62-0.72. The three species of parasitoid spread evenly in all districts and cities in Bali according to the host distribution map, namely P. manihoti on cassava crop. The four parasitoids showed varying parasitic levels in the field with the highest parasitization rate was A. lopezi followed by Acerophagus sp., Blepyrus sp., and Encarsia sp.


Abduchalek B. 2016. Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae): Geographic Distribution in Java and Initiation of Biological Control. [Thesis]. Bogor (ID): Institut Pertanian Bogor. [Indonesian].
Adriani E. 2016. Preference, Suitability, and Parasitism of Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae) on Various Instars of Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). [Thesis]. Bogor (ID): Institut Pertanian Bogor. [Indonesian].
Altieri MA. 1999. The ecological role of biodiversity in agroecosystems. J Agric Ecosyst Environ 4. 19-31.
Altieri MA. Nicholls CI. 2004. Biodiversity and Pest Management in Agroecosystems. Haworth Press, New York.
Andow DA. 1991. Vegetational diversity and arthropod population response. Ann Rev Entomol 36. 561-586.
Attia AR. 2012. Hymenopterous parasitoids as a bioagents for controlling mealybugs (Hemiptera: Pseudococcidae) in Egypt [review]. J Biolog Sci. 5(3): 183-192.
Aquilino KM, Cardinale BJ, Ives AR. 2005. Reciprocal Effects Of Host Plant and Natural Enemy Diversity on Herbivore Suppresion: an Emoirical Study of a Model Tritrophic System. Oikos 108. 275-282.
Baggen LR, Gurr GM. 1998. The influence of food on Capidosoma koehleri (Hymenoptera: Encyrtidae), and the use of flowering plants as habitat management tool to enhance biological controlof potato moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). Bio Cont. 11. 9-17.
Balai Penelitian Tanaman Aneka Kacang dan Umbi. 2005. Varieties of Cassava.
Barbosa P, Benrey B. 1998. The influence of plants on insec parasitoids: implication for conservation biological control. In: Barbosa P (Ed). Conservation Biological Control. Academic Press, San Diego
Dwianri. 2013. Cassava Farmers’ Practices and Perceptions of the Mealybug Phenacoccus manihoti in District of Bogor [Skription]. Bogor (ID): Institut Pertanian Bogor. [Indonesian].
Giardanengo P, Nenon JP. 1990. Melanization and encapsulation of eggs and larvae of Epidinocarsis lopezi by its host Phenacoccus manihoti; effect of superparasitism and egg laying patterns. Entomol Exp Appl. 56(2):155-163.
Godfray HCJ. 1994. Parasitoids Behavioral and Evolutionary Ecology. New Jersey (USA): Princeton University Press.
Gutierrez AP, Neuenschwander P, Schulthess F, Herren HR, Baumgartner JU, Wermelinger B, Lohr B, dan Ellis CK. 1988. Analysis of biological control of cassava pests in Africa: II. Cassava mealybug Phenacoccus manihoti. appl. Ecol. 25. 921-940.
Gurr GM, Wretten SD, Altieri MA. 2004. Ecology Engineering for pest management. CABI Publishing, Wallingford.
Haye T, Goulet H, Mason PG, Kuhlmann U. 2005. Does fundamental host range match ecological host range. A restrospective case study of a Lygus plant bug parasitoid. Biological Control 35. 55-67
Herren HR, Neuenschwander P, Hennessey RD, Hammond WNO. 1987. Introduction and dispersalof Epidinocarsis lopezi (Hym., Encyrtidae), anexotic parasitoid of the cassava mealybug, Phenacoccus manihoti (Hom., Pseudococcidae),in Africa.Agr. Ecosys. Environ. 19(2): 131-144.
James B, Yaninek J, Neuenschwander P, Cudjoe A, Modder W, Echendu N, Toko M. 2000. Pest Control in Cassava Farms. Nigeria (NG): Wordsmithes Printers Lagos.
Karyani RD. 2015. Host Suitability Test of Parasitoid Anagyrus lopezi De Santis (Hymenoptera: Encyrtidae) for Mealybugs Species Associated with Cassava (Manihot esculenta Crantz). [Thesis]. Bogor (ID): Institut Pertanian Bogor. [Indonesian].
Le Ru B, Fabres G. 1986. Influence de la temperature et de l'hygrometrie relative sur le taux d'accroissement des populations de la cochenille du manioc, Phenacoccus manihoti (Horn. Pseudococcidae) au Congo. In "La cochenille du manioc et sa biocoenose au Congo 1979-1984". Travaux de Vequipe Franco-Congolaise ORSTOMDGRS, Brazzaville, BP 181, RP du Congo. 39-55.
Lohr B,Varela AM. 1990. Exploration for natural enemies of the cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae), in South America for the biological control of this introduced pest in Africa. Bulletin of Entomological Research. 80. 417-425.
Magurran AE. 2005. Measuring Biological Diversity. Blackwell Publishing. Oxford, UK.
Maple JD. 1947. The eggs and first instar larvae of Encyrtidae and their morphological adaptions for respiration. In: Noyes JS, Hayat M, editor. Oriental Mealybug Parasitoids of the Anagyrini; 1994; Cambridge (GB): University Press.
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 Agr and Urban Entomol. 26(4): 167-174.
Nicholls CI, Alfieri MA. 2003. Designing spesies-rich, pest-suppresive agroecosystem through habitat management. Http://
Neuenschwander P. 1994. Control of cassava mealybugs in Africa: lessons from a biological control project. African Crops Sci J. 12(4): 369-383.
Neuenschwander P. 2001. Biological control of the cassava mealybug in Africa: A review. Biological Control. 21. 214-229.
Noyes JS, Schauff ME. 2003. New Encyrtidae (Hymenoptera) from papaya mealybug (Paracoccus marginatus Williams and Granara de Willink) (Hemiptera: Sternorrhyncha: Pseudococcidae). Proc Entomol Soc. Washington. 105. 180-185.
Noyes JS. 2000. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), The subfamily Tetracneminae, parasitoids of mealybugs (Homoptera: Pseudococcidae). Memoirs of the American Entomological Institute.
Noyes JS, Hayat M. 1994. Oriental Mealybug Parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). Cambridge (GB): University Press.
Nwanze KF. 1982. Relationship between cassava root yields and crop infestationsby the mealybug, Phenacoccus manihoti. Trop Pest Manag. 28. 27-32.
Odebiyi JA, Bokonon-Ganta AH. 1986. Biology of Epidinocarsis [Apoanagyrus] lopezi [Hymenoptera: Encyrtidae] an exotic parasitoid cassava mealybug, Phenacoccus manihoti [Homoptera: Pseudococcidae] in Nigeria. Entomophaga. 3(3): 251-260.
Paulsen HM, Schochow M, Ulber B, Kühneand S, Rahmann G. 2006. Mixed cropping systems for biological control of weeds and pests in organic oilseed crops. COR 2006, Aspects of Applied Biology. 215-220.
Phillips CB. 1998. Influence of liquid food and fecundity and longevity of Microtonus hyperodae Loan. Http://
Purnomo H. 2010. Pengantar Pengendalian Hayati. Yogyakarta (ID): ANDI OFFSET.
Rauf A, Shepard BM, Jhonson MW. 2000. Leafminer in vegetables, ornamental plants and weeds in indonesia: surveys of host crops, species composition and parasitoids. Intl J Pest Manag 48(4): 257-266.
Riyanto. 2010. How Insects Break Plant Defense. Forum MIPA 13(1): 1-9.
Robinson RA, Sutherland WJ. 2002. Post-War Changesin Arable Farming and Biodiversity in Great Britain. J. Appl. Ecol. 39. 157-176.
Schulthess F, Baumgartner JU, Delucchi V, Guttierez AP. 1991. The influence of the cassava mealybug, Phenacoccus manihoti Mat-Ferr (Homoptera: Psedococcidae) on yield formation of cassava, Manihot esculanta Crantz. J Appl Entomol. 111. 155-165.
Sivinski J, Pinero J, Aluja M. 2000. The distribution of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracrus, Mexico. Bio Control 18. 258-269.
Souissi R, Le Ru B. 1999. Behavioral responses of the endoparasitoid Apoanagyrus lopezi to odours of the host and host’s cassava plants. Entomol Exp Appl. 90(2): 215-220.
Supartha IW. 2003. Parasitoids fauna diversity of Liriomyza spp. on vegetable crop in Bali and Lombok of Indonesia. 4th Congress of Indonesian Entomological Society and Symposium 2003. Cipayung Bogor (Indonesia) 3-7 March 2003. [Indonesian].
Supartha IW, Bagus IGN, Sudiarta P. 2005. Population abundance of Liriomyza spp. (Diptera: Agromyzidae) and parasitoids on highland vegetables crop. Agritrop 24(2): 51-5.9 [Indonesian]
Syamsudin H. 2008. Distribution of Hemiptarsenus varicornis Girault (Hymenoptera: Eulopidae), Larval Parasitoid of Liriomyza spp. (Diptera: Agromyzidae). Lembaga Pertanian Sehat, Jakarta [Indonesian].
Ubaidillah R. 2003. Parasitoid wasps of Eulophinae (Hymenoptera: Eulophidae) in East Lesser Sunda, Indonesia. Treubia 33(1): 43-70.
Untung K. 2010. Diktat Basics of Plant Pest Sciences. Faculty of Agriculture Gajah Mada University. [Indonesian].
Van Alphen JMM, Jervis MA. 1996. Foraging behaviour. In: Jervis MA, Kidd N, editor: Insect Natural Enemies: Practical Approaches to their Study and Evaluation. Cradiff (UK): Springer science.
Van Driesche RG, Hoddle M, Center T. 2008. Control of Pests and Weeds by Natural Enemies: an Introduction to Biological Control. Victoria (AU): Blackwell Publishing.
Wahyuni S. 2017. Community Structure and Potential of Parasitoid in Regulating Population Liriomyza spp. (Diptera: Agromyzidae) in Vegetable Crop in Leser Sunda Island. [Dissertation]. Denpasar. UNUD. [Indonesian].
Wahyuni S, Supartha IW, Ubaidilah R, Wijaya IN. 2017. Parasitoid Community Structure of Leafeminer Liriomyza spp. (Diptera: Agromizidae) and Rate Of Parasitization on Vegetable Crop in Leser Sunda Island, Indonesia. Biodiversitas Journal of Biological Diversity. 18(2): 593-600. [Indonesian].
Wardani N, Rauf A, Winasa IW, Santoso S. 2014. The life history and population growth parameters of mealybug Phenacoccus manihoti Matile-Ferrero (Hemiptera:Pseudococcidae) on two cassava varieties. J HPT Tropika. 14(1): 64-70. [Indonesian].
Wardani N. 2015. Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae), A Newly Invasive Pest in Indonesia. [Dissertation]. Bogor (ID): Institut Pertanian Bogor. [Indonesian].
Warsito. 2004. Diversity, Abundance and Role of Natural Enemies Leafminer Liriomyza huidobrensis (Blancard) (Diptera: Agromysidae) in Potatoes Plant Solanum tuberosum L. [Thesis]. Bogor : Institut Pertanian Bogor. [Indonesian].
Winotai A, Goergen G, Tamò M, Neuenschwander P. 2010. Cassava mealybug has reached Asia. Biocontrol News Inf. 31: 10N–11N. Doi: 10.1017/s0007485300050677

Most read articles by the same author(s)