Journal of Pest Science

, Volume 91, Issue 4, pp 1199–1211 | Cite as

Effective biological control of an invasive mealybug pest enhances root yield in cassava

  • A. Thancharoen
  • S. Lankaew
  • P. Moonjuntha
  • T. Wongphanuwat
  • B. Sangtongpraow
  • R. Ngoenklan
  • P. Kittipadakul
  • Kris A. G. WyckhuysEmail author
Original Paper


Insects provide critical ecosystem services to humanity, including biological control of pests. Particularly for invasive pests, biological control constitutes an environmentally sound and cost-effective management option. Following its 2008 invasion of Southeast Asia, biological control was implemented against the cassava mealybug Phenacoccus manihoti (Hemiptera: Pseudococcidae) through the introduction and subsequent release of the host-specific parasitoid Anagyrus lopezi (Hymenoptera: Encyrtidae) in Thailand. In this study, we quantify yield benefits of mealybug biological control in Thailand’s cassava crop by using two different types of manipulative field trials: i.e., ‘physical exclusion’ cage trials and field-level ‘chemical exclusion’ assays. In cage trials with two popular cassava varieties, root yield and total dry matter (or ‘biological yield’) were a respective 4.0–4.2 times and 3.5–3.9 times higher in the presence of biological control. Extrapolating results from cage trials, biological control thus ensured an approximate yield gain of 5.3–10.0 T/ha for either variety. Under chemical exclusion trials, P. manihoti populations attained levels of 3266 ± 1021 cumulative mealybug-days (CMD) over a 10-month time period, and no longer impact yields. Moreover, under effective P. manihoti control, both root yield and biological yield increased with season-long CMD measures, and pest management interventions-including insecticide sprays-led to notable reductions in yield. This study is the first to show how biological control effectively downgrades the globally invasive P. manihoti to non-economic status and restores yields in Thailand’s cassava crop. Our work emphasizes the economic value of biological control, reveals how current P. manihoti populations do not necessarily cause yield penalties, and underlines the central importance of nature-based approaches in intensifying global agricultural production.


Biological control Biodiversity Sustainable intensification Food security Ecosystem services Natural enemies 



This manuscript is the result of fully collaborative research, with trials jointly conceptualized, defined and executed by Thai counterparts and CIAT personnel. We would like to thank Dr. Sutkhet Nakasathien at Kasetsart University, and Dr. Prapit Wongtiem and senior administrators at the Thai Department of Agriculture for facilitating this work and encouraging graduate students and junior research staff. We are also grateful to Dr. James Cock for revising an earlier draft of the manuscript. This initiative was conducted as part of an EC-funded, IFAD-managed, CIAT-executed programme (CIAT-EGC-60-1000004285), while additional funding was also provided through the CGIAR-wide Research Program on Roots, Tubers and Banana (CRP-RTB).


This study was conducted as part of an EC-funded, IFAD-managed, CIAT-executed programme (CIAT-EGC-60-1000004285), while additional funding was provided through the CGIAR-wide Research Program on Roots, Tubers and Banana (CRP-RTB).

Compliance with ethical standards

Conflict of interest

All authors declare that there are no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Andrews KL, Bentley JW, Cave RD (1992) Enhancing biological control’s contributions to integrated pest management through appropriate levels of farmer participation. Fla Entomol 75:429–439CrossRefGoogle Scholar
  2. Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Philos Trans R Soc Lond B 363:761–776CrossRefGoogle Scholar
  3. Bebber DP, Ramotowski MAT, Gurr SJ (2013) Crop pests and pathogens move polewards in a warming world. Nat Clim Change 3:985–988CrossRefGoogle Scholar
  4. Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238CrossRefPubMedGoogle Scholar
  5. Bradshaw CJA, Leroy B, Bellard C, Roiz D, Albert C, Fournier A, Barbet-Massin M, Salles JM, Simard F, Courchamp F (2016) Massive yet grossly underestimated global costs of invasive insects. Nat Commun 7:12986CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cock JH (1978) A physiological basis of yield loss in cassava due to pests. In: Brekelbaum T, Bellotti A, Lozano JC (eds) Proc. cassava protection workshop. CIAT, Cali, Colombia, pp. 9–16Google Scholar
  7. Cock JH (1984) Cassava. In: Goldsworthy PR, Fisher NM (eds) The physiology of tropical field crops. Wiley, New York, pp 529–549Google Scholar
  8. Cock JH (2012) Cassava growth and development. In: Howeler RH (ed) The cassava handbook: a reference manual. International Center for Tropical Agriculture CIAT, Cali, pp 39–61Google Scholar
  9. Cock MJW, Murphy ST, Kairo MTK, Thompson E, Murphy RJ, Francis AW (2016) Trends in the classical biological control of insect pests by insects: an update of the BIOCAT database. Biocontrol 61:349–363CrossRefGoogle Scholar
  10. Connor DJ, Cock JH, Parra GE (1981) Response of cassava to water shortage. I. Growth and yield. Field Crops Res 4:181–200CrossRefGoogle Scholar
  11. Constanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260CrossRefGoogle Scholar
  12. Costamagna AC, Landis DA, DiFonzo CD (2007) Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans. Ecol Appl 17:441–451CrossRefPubMedGoogle Scholar
  13. Cullen R, Warner KD, Jonsson M, Wratten SD (2008) Economics and adoption of conservation biological control. Biol Control 45:272–280CrossRefGoogle Scholar
  14. Daily GC, Polasky S, Goldstein J, Kareiva PM, Mooney HA, Pejchar L, Ricketts TH, Salzman J, Shallenberger R (2009) Ecosystem services in decision making: time to deliver. Front Ecol Environ 7:21–28CrossRefGoogle Scholar
  15. DeBach P, Huffaker CB (1971) Experimental techniques for evaluation of the effectiveness of natural enemies. In: Huffaker CB (ed) Biological control. Springer, Boston, pp 113–140Google Scholar
  16. DeClercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. Biocontrol 56:681–698CrossRefGoogle Scholar
  17. Delaquis E, de Haan S, Wyckhuys KAG (2017) On-farm diversity offsets environmental pressures in tropical agro-ecosystems: a synthetic review for cassava-based systems. Agric Ecosyst Environ 251:226–235CrossRefGoogle Scholar
  18. Fermont AM, Van Asten PJ, Tittonell P, Van Wijk MT, Giller KE (2009) Closing the cassava yield gap: an analysis from smallholder farms in East Africa. Field Crops Res 112:24–36CrossRefGoogle Scholar
  19. Gardiner MM, Landis DA, Gratton C, DiFonzo CD, O’Neal M, Chacon JM et al (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19:143–154CrossRefPubMedGoogle Scholar
  20. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987CrossRefGoogle Scholar
  21. Graziosi I, Wyckhuys KAG (2017) Integrated management of arthropod pests of cassava: the case of Southeast Asia. In: Hershey C (ed) Achieving sustainable cultivation of cassava, vol II. Burleigh Dodds, Cambridge, p 300Google Scholar
  22. Graziosi I, Minato N, Alvarez E, Ngo DT, Hoat TX, Aye TM, Pardo JM, Wongtiem P, Wyckhuys KAG (2016) Emerging pests and diseases of South-east Asian cassava: a comprehensive evaluation of geographic priorities, management options and research needs. Pest Manag Sci 72:1071–1089CrossRefPubMedGoogle Scholar
  23. Gutierez AP, Neuenschwander P, Schulthess F, Herren HR, Baumgartner JU, Wermelinger B, Lohr B, Ellis CK (1988) Analysis of biological control of cassava pests in Africa. II. Cassava mealybug Phenacoccus manihoti. J Appl Ecol 25:921–940CrossRefGoogle Scholar
  24. Gutierez AP, Caltagirone LE, Meikle W (1999) Evaluation of results. Economics of biological control. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic Press, San Diego, pp 243–252CrossRefGoogle Scholar
  25. Hajek AE, Hurley BP, Kenis M, Garnas JR, Bush SJ, Wingfield MJ, van Lenteren JC, Cock MJW (2016) Exotic biological control agents: a solution or contribution to arthropod invasions. Biol Invasions 18:953–969CrossRefGoogle Scholar
  26. Hallmann CA, Song M, Jongejans E, Siepel H, Hofland N, Schwan H, Stenmans W, Muller A, Sumser H, Horren T, Goulson D, de Kroon H (2017) More than 75% decline over 27 years in total flying insect biomass in protected area. PLoS ONE 12(10):e0185809CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058CrossRefGoogle Scholar
  28. Hovick SM, Carson WP (2015) Tailoring biocontrol to maximize top-down effects: on the importance of underlying site fertility. Ecol Appl 25:125–139CrossRefPubMedGoogle Scholar
  29. Hough-Goldstein J, Schiff M, Lake E, Butterworth B (2008) Impact of the biological control agents Rhinoncomimus latipes (Coleoptera: Curculionidae) on mile-a-minute weed, Persicaria perfoliata, in field cages. Biol Control 46, 417–423CrossRefGoogle Scholar
  30. Howeler R (2014) Sustainable soil and crop management of cassava in Asia. International Center for Tropical Agriculture, CIAT, Cali, p 280Google Scholar
  31. Karlström A, Calle F, Salazar S, Morante N, Dufour D, Ceballos H (2016) Biological implications in cassava for the production of amylose-free starch: impact on root yield and related traits. Front Plant Sci 7:604CrossRefPubMedPubMedCentralGoogle Scholar
  32. Karp DS, Mendenhall CD, Sandi RF, Chaumont N, Ehrlich PR, Hadly EA, Daily GC (2013) Forest bolsters bird abundance, pest control and coffee yield. Ecol Lett 16:1339–1347CrossRefPubMedGoogle Scholar
  33. LaCanne CE, Lundgren JG (2018) Regenerative agriculture: merging farming and natural resource conservation profitably. PeerJ 6:e4428CrossRefPubMedPubMedCentralGoogle Scholar
  34. Landau S, Everitt BS (2004) A handbook of statistical analyses using SPSS. Chapman and Hall/CRC, Boca RatonGoogle Scholar
  35. Landis DA, Gardiner M, van der Werf W, Swinton SM (2008) Increasing corn for biofuel production reduces biocontrol services in agricultural landscapes. Proc Natl Acad Sci USA 105:20552–20557CrossRefPubMedGoogle Scholar
  36. Le TTN, Graziosi I, Cira TM, Gates MW, Wyckhuys KAG (2018) Landscape context does not constrain biological control of Phenacoccus manihoti in intensified cassava systems of southern Vietnam. Biol Control 121:129–139CrossRefGoogle Scholar
  37. Losey J, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323CrossRefGoogle Scholar
  38. Lundgren JG, Fausti SW (2015) Trading biodiversity for pest problems. Sci Adv 1:e1500558CrossRefPubMedPubMedCentralGoogle Scholar
  39. Madhaiyan M, Poonguzhali S, Hari K, Saravanan VS, Sa T (2006) Influence of pesticides on the growth rate and plant-growth promoting traits of Gluconacetobacter diazotrophicus. Pestic Biochem Phys 84:143–154CrossRefGoogle Scholar
  40. Martínez-Blay V, Pérez-Rodríguez J, Tena A, Soto A (2018) Density and phenology of the invasive mealybug Delottococcus aberiae on citrus: implications for integrated pest management. J Pest Sci 91:625–637CrossRefGoogle Scholar
  41. Melo FPL, Arroyo-Rodriguez V, Fahrig L, Martinez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:462–468CrossRefPubMedGoogle Scholar
  42. Messing RH, Wright MG (2006) Biological control of invasive species: Solution or pollution? Front Ecol Environ 4:132–140CrossRefGoogle Scholar
  43. Muniappan R, Sheppard BM, Watson GW, Carner GR, Rauf A, Sartiami D et al (2009) New records of invasive insects (Hemiptera: Sternorrhyncha) in Southeast Asia and West Africa. J Agric Urban Entomol 26:167–174CrossRefGoogle Scholar
  44. Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:1–25CrossRefGoogle Scholar
  45. Neuenschwander P, Schulthess F, Madojemu E (1986) Experimental evaluation of the efficiency of Epidinocarsis lopezi, a parasitoid introduced into Africa against the cassava mealybug Phenacoccus manihoti. Entomol Exp Appl 42:133–138CrossRefGoogle Scholar
  46. Neuenschwander P, Hammond WNO, Guttierez AP, Cudjoe AR, Adjakloe R, Baumgartner JU, Regev U (1989) Impact assessment of the biological control of the cassava mealybug, Phenacoccus manihoti Matile Ferrero (Hemiptera: Pseudococcidae) by the introduced parasitoid Epidinocarsis lopezi (De Santis) (Hymenoptera: Encyrtidae). Bull Entomol Res 79:579–594CrossRefGoogle Scholar
  47. Norgaard RB (1988) The biological control of cassava mealybug in Africa. Am J Agric Econ 70:366–371CrossRefGoogle Scholar
  48. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43CrossRefGoogle Scholar
  49. Oliver TH, Isaac NJ, August TA, Woodcock BA, Roy DB, Bullock JM (2015) Declining resilience of ecosystem functions under biodiversity loss. Nat Commun 6:10122CrossRefPubMedPubMedCentralGoogle Scholar
  50. Paini DR, Sheppard AW, Cook DC, De Barro PJ, Worner SP, Thomas MB (2016) Global threat to agriculture from invasive species. Proc Natl Acad Sci USA 113:7575–7579CrossRefPubMedGoogle Scholar
  51. Qureshi JA, Stansly PA (2009) Exclusion techniques reveal significant biotic mortality suffered by Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) populations in Florida citrus. Biol Control 50:129–136CrossRefGoogle Scholar
  52. Ragsdale DW, McCornack BP, Venette RC, Potter BD, MacRae IV, Hodgson EW et al (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). J Econ Entomol 100:1258–1267CrossRefPubMedGoogle Scholar
  53. Sartiami D, Watson GW, Roff MNM, Hanifah MY, Idris AB (2015) First record of cassava mealybug, Phenacoccus manihoti (Hemiptera: Pseudococcidae), in Malaysia. Zootaxa 3957:235–238CrossRefPubMedGoogle Scholar
  54. Schreinemachers P, Afari-Sefa V, Heng CH, Dung PTM, Praneetvatakul S, Srinivasan R (2015) Safe and sustainable crop protection in Southeast Asia: status, challenges and policy options. Environ Sci Policy 54:357–366CrossRefGoogle Scholar
  55. Schulthess F, Baumgartner JU, Delucchi V, Gutierez AP (1991) The influence of the cassava mealybug Phenacoccus manihoti Mat.-Ferr. (Homoptera, Pseudococcidae) on yield formation of cassava, Manihot esculenta Crantz. J Appl Entomol 111:155–165CrossRefGoogle Scholar
  56. Seastedt TR (2014) Biological control of invasive plant species: a reassessment for the Anthropocene. New Phytol 205:490–502CrossRefPubMedGoogle Scholar
  57. Snyder WE, Wise DH (2001) Contrasting trophic cascades generated by a community of generalist predators. Ecology 82:1571–1583CrossRefGoogle Scholar
  58. Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9:e84847CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tamburini G, Lami F, Marini L (2017) Pollination benefits are maximized at intermediate nutrient levels. Proc R Soc Lond B 284:20170729CrossRefGoogle Scholar
  60. Tittonell P, Giller KE (2013) When yield gaps are poverty traps: the paradigm of ecological intensification in African smallholder agriculture. Field Crops Res 143:76–90CrossRefGoogle Scholar
  61. Van Driesche R, Hoddle M, Center T (2008) Control of pests and weeds by natural enemies. Blackwell Publishing Limited, Malden, p 484Google Scholar
  62. Van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L et al (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54:S2–S33CrossRefGoogle Scholar
  63. van Lenteren JC (1980) Evaluation of control capabilities of natural enemies: Does art have to become science? Neth J Zool 30:369–381CrossRefGoogle Scholar
  64. van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634CrossRefPubMedGoogle Scholar
  65. Warner KD, Daane KM, Getz CM, Maurano SP, Calderon S, Powers KA (2011) The decline of public interest agricultural science and the dubious future of crop biological control in California. Agric Human Values 28:483–496CrossRefGoogle Scholar
  66. Wilde G, Roozeboom K, Claassen M, Sloderbeck P, Witt M, Janssen K, Harvey T, Kofoid K, Brooks L, Shufran R (1999) Does the systemic insecticide imidacloprid (Gaucho) have a direct effect on yield of grain sorghum? J Prod Agric 12:382–389CrossRefGoogle Scholar
  67. Wilson EO (2017) Biodiversity research requires more boots on the ground. Nat Ecol Evol 1:1590–1591CrossRefPubMedGoogle Scholar
  68. Winotai A, Goergen G, Tamo M, Neuenschwander P (2010) Cassava mealybug has reached Asia. Biocontrol News Inf 31:10N–11NGoogle Scholar
  69. Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG, Redhead J, Ridding L et al (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356:1393–1395CrossRefPubMedGoogle Scholar
  70. Wyckhuys KAG, Rauf A, Ketelaar J (2015) Parasitoids introduced into Indonesia: part of a region-wide campaign to tackle emerging cassava pests and diseases. Biocontrol News Inf 35:29N–38NGoogle Scholar
  71. Wyckhuys KAG, Burra DD, Tran DH, Graziosi I, Walter AJ, Nguyen TG, Trong HN, Le BV, Le TNN, Fonte SJ (2017a) Soil fertility regulates invasive herbivore performance and top-down control in tropical agro-ecosystems of Southeast Asia. Agric Ecosyst Environ 249:38–49CrossRefGoogle Scholar
  72. Wyckhuys KAG, Graziosi I, Burra DD, Walter AJ (2017b) Phytoplasma infection of a tropical root crop triggers bottom-up cascades by favoring generalist over specialist herbivores. PLoS ONE 12(8):e0182766CrossRefPubMedPubMedCentralGoogle Scholar
  73. Wyckhuys KAG, Orankanok W, Rauf A, Ketelaar JW, Georgen G, Neuenschwander P (2018) Biological control: cornerstone of AW-IPM programs for the cassava mealybug in Southeast Asia. Area-wide Pest Management of Insect Pests, UN-FAO/IAEA, Vienna (in press)Google Scholar
  74. Yaninek Y, Gutierrez AP, Herren HR (1990) Dynamics of Mononychellus tanajoa (Acari: Tetranychidae) in Africa: effects on dry matter production and allocation in cassava. Environ Entom 19, 1767–1772CrossRefGoogle Scholar
  75. Zeddies J, Schaab RP, Neuenschwander P, Herren HR (2001) Economics of biological control of cassava mealybug in Africa. Agric Econ 24:209–219CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Entomology, Faculty of AgricultureKasetsart UniversityBangkokThailand
  2. 2.Department of AgricultureRayong Field Crops Research Center, Field Crops Research Institute (FCRI)RayongThailand
  3. 3.Department of Agronomy, Faculty of AgricultureKasetsart UniversityBangkokThailand
  4. 4.CGIAR Program on Roots, Tubers and Banana (CRP-RTB)International Center for Tropical Agriculture CIATHanoiVietnam
  5. 5.International Joint Research Laboratory on Ecological Pest ManagementFuzhouPeople’s Republic of China
  6. 6.University of QueenslandBrisbaneAustralia
  7. 7.Institute of Plant Protection, Chinese Academy of Agricultural SciencesBeijingPeople’s Republic of China

Personalised recommendations