Journal of Pest Science

, Volume 86, Issue 3, pp 387–398 | Cite as

The invasive mealybug Maconellicoccus hirsutus: lessons for its current range expansion in South America and invasive pest management in general

  • Mark P. Culik
  • Maurício José Fornazier
  • David dos Santos Martins
  • José Salazar ZanuncioJr.
  • José Aires Ventura
  • Ana Lúcia B. G. Peronti
  • José Cola Zanuncio
Review

Abstract

The invasive mealybug Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) is a plant feeding insect believed to be native to Southern Asia or Australia. This mealybug has become established in many regions throughout the world (including the Caribbean and North America) in the past 100 years and is currently expanding its range in South America. Because this insect is of concern as a potential pest of many plant species, this review is provided to summarize knowledge of M. hirsutus based on past research that may be most useful for addressing the current invasion of South America by the species, and to identify gaps in information that may need to be addressed to inhibit the spread of the insect and improve management methods for this and similar organisms. In most areas into which M. hirsutus has expanded its range it is commonly suppressed by native or introduced natural enemies. Therefore, besides preventing introduction, establishment and spread of this potential pest, efforts should be made to determine if natural enemies of M. hirsutus are present in areas of concern (i.e., where the mealybug may be introduced and become established). Such information will enable determination of the need for introduction or augmentation of biological control agents in response to possible entry and establishment of the mealybug in new areas. Methods developed in response to the recent invasion of the Caribbean and North America by M. hirsutus may serve as models for addressing the threat of this and similar invasive pests in South America and elsewhere.

Keywords

Neotropical Biodiversity Biological control Natural enemies Geographic distribution Integrated pest management (IPM) 

References

  1. Abd-Rabou S (2008) Updated list of the parasitoids attacking mealybugs (Hemiptera: Pseudococcidae) in Egypt. In: Branco M, Franco JC, Hodgson CJ (eds) Proceedings of the XI international symposium on scale insect studies, Oeiras, Portugal, September 2007. ISA Press, Lisbon, pp 235–240Google Scholar
  2. Abd-Rabou S, Shalaby H, Germain JF, Ris N, Kreiter P, Malausa T (2012) Identification of mealybug pest species (Hemiptera: Pseudococcidae) in Egypt and France, using a DNA barcoding approach. Bull Entomol Res 24:1–9Google Scholar
  3. Aristizábal LF, Mannion C, Bergh C, Arthurs S (2012) Life history of pink hibiscus mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) on three Hibiscus rosa-sinensis cultivars. Fla Entomol 90:440–446Google Scholar
  4. Ben-Dov Y, Miller DR, Gibson GAP (2012) ScaleNet. http://www.sel.barc.usda.gov/scalenet/scalenet.htm. Accessed 14 Sept 2012
  5. Bento JMS, de Moraes GJ, de Matos AP, Bellotti AC (2000) Classical biological control of the mealybug Phenacoccus herreni (Hemiptera: Pseudococcidae) in northeastern Brazil. Environ Entomol 29:355–359CrossRefGoogle Scholar
  6. CABI/EPPO (2004) Maconellicoccus hirsutus. Distribution maps of plant pests No. 100. CAB International, WallingfordGoogle Scholar
  7. Castle SJ, Prabhaker N (2011) Field evaluation of two systemic neonicotinoid insecticides against pink hibiscus mealybug (Maconellicoccus hirsutus (Green)) on mulberry trees. J Pest Sci 84:363–371CrossRefGoogle Scholar
  8. Cermeli M, Valles PM, Godoy F, Romero R, Cárdenas O (2002) Presencia de la cochinilla rosada de la cayena Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) en Venezuela. Entomotropica 17(1):103–105Google Scholar
  9. Chong JH (2009) First report of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), in South Carolina. J Agric Urban Entomol 26):87–94Google Scholar
  10. Chong JH, Roda AL, Mannion CM (2008) Life history of the mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), at constant temperatures. Environ Entomol 37(2):323–332PubMedCrossRefGoogle Scholar
  11. Culik MP, Martins D dos S, Ventura JA (2011) New distribution and host records of chalcidoid parasitoids (Hymenoptera: Chalcidoidea) of scale insects (Hemiptera: Coccoidea) in Espírito Santo, Brazil. Biocontrol Sci Tech 21:877–881Google Scholar
  12. Daane KM, Almeida RPP, Bell VA, Walker JTS, Botton M, Fallahzadeh M, Mani M, Miano JL, Sforza R, Walton VM, Zaviezo T (2012) Biology and management of mealybugs in vineyards. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards: pests, approaches, and future directions. Springer, Dordrecht, pp 271–307CrossRefGoogle Scholar
  13. De Lotto G (1954) Three apparently new mealy bugs from Kenya. Proc R Entomol Soc Lond 23:110–114Google Scholar
  14. FAO (2011) Pest risk analysis for quarantine pests including analysis of environmental risks and living modified organisms. https://www.ippc.int/file_uploaded/1323945243_ISPM_11_2004_En_2011-11-29_Refor.pdf. Accessed 14 Mar 2013
  15. Francis A, Bloem KA, Roda AL, Lapointe SL, Zhang A, Onokpise O (2007) Development of trapping methods with a synthetic sex pheromone of the pink hibiscus mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae). Fla Entomol 90:440–446CrossRefGoogle Scholar
  16. Gajadin N (2004) Control of the hibiscus mealy bug (Maconellicoccus hirsutus) in Suriname: a comparative study of the chemical and biological control. BSc Thesis, Anton de Kom University of SurinameGoogle Scholar
  17. García-Valente F, Ortega-Arenas LD, González-Hernández H, Villanueva-Jiménez JA, López-Collado J, González-Hernández A, Arredondo-Bernal HC (2009) Parasitismo natural e inducido de A. kamali sobre la cochinilla rosada en brotes de teca, en Bahía de Banderas, Nayarit. Agrociencia 43:729–738Google Scholar
  18. González FG (2012) Coccinellidae de Brasil. http://www.coccinellidae.cl/paginasWebBra/Paginas/Cryptolaemus_montrouzieri_Bra.php. Accessed 11 Mar 2013
  19. González-Gaona E, Sánchez-Martínez G, Zhang A, Lozano-Gutiérrez J, Carmona-Sosa F (2010) Validación de dos compuestos feromonales para el monitoreo de la cochinilla rosada del hibisco en México. Agrociencia 44:65–73Google Scholar
  20. Goolsby JA, Kirk AA, Meyerdirk DE (2002) Seasonal phenology and natural enemies of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in Australia. Fla Entomol 85(3):494–498CrossRefGoogle Scholar
  21. Hall DG, Roda A, Lapointe SL, Hibbard K (2008) Phenology of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in Florida based on attraction of adult males to pheromone traps. Fla Entomol 91:305–310CrossRefGoogle Scholar
  22. Hara AH, Jacobsen CM (2005) Hot water immersion for surface disinfestations of Maconellicoccus hirsutus (Homoptera: Pseudococcidae). J Econ Entomol 98:284–288PubMedCrossRefGoogle Scholar
  23. IPPC (2013) Latin America & Caribbean. https://www.ippc.int/index.php?id=37229&L=0. Accessed 13 Mar 2013
  24. Jara V, Meza FJ, Zaviezo T, Chorbadjian R (2012) Climate change impacts on invasive potential of pink hibiscus mealybug, Maconellicoccus hirsutus (Green), in Chile. Climatic Change. http://www.springerlink.com/content/t3x267137254861v/fulltext.pdf?MUD=MP. Accessed 9 Nov 2012
  25. Kairo MTK, Pollard GV, Peterkin DD, Lopez VF (2000) Biological control of the hibiscus mealybug, Maconellicoccus hirsutus Green (Hemiptera: Pseudococcidae) in the Caribbean. Integr Pest Manag Rev 5(4):241–254CrossRefGoogle Scholar
  26. Katke M (2008) Seasonal incidence, biology and management of grape mealy bug, Maconellicoccus hirsutus (Green)(Homoptera: Pseudococcidae). Masters Thesis, University of Agricultural Sciences, Dharwad 89 ppGoogle Scholar
  27. Kondo T, Ramos-Portilla AA, Vergara-Navarro EV (2008) Updated list of mealybugs and putoids from Colombia (Hemiptera: Pseudococcidae and Putoidae). Boletin del Museo de Entomologia de la Universidad del Valle 9(1):29–53Google Scholar
  28. Krishnamoorthy A, Mani M (1989) Records of green lacewings preying on mealybugs in India. Curr Sci 58(3):155–156Google Scholar
  29. Machado da Costa J, Williams RN, Schuster MF (1970) Rhodesgrass scale, Antonina graminis, in Brazil. II. Introduction of Neodumetia sangwani, natural enemy of rhodesgrass scale. Pesq Agropec Bras 5:15–24Google Scholar
  30. Malausa T, Fenis A, Warot S, Germain J-F, Ris N, Prado E, Botton M, Vanlerberghe-Masutti F, Sforza R, Cruaud C, Couloux A, Kreiter P (2011) DNA markers to disentangle complexes of cryptic taxa in mealybugs (Hemiptera: Pseudococcidae). J Appl Entomol 135:142–155CrossRefGoogle Scholar
  31. Marsaro AL Jr., Peronti ALBG, Penteado-Dias AM, Morais EGF, Pereira PRVS (2013) First report of Maconellicoccus hirsutus (Green, 1908) (Hemiptera: Coccoidea: Pseudococcidae) and the associated parasitoid Anagyrus kamali Moursi, 1948 (Hymenoptera: Encyrtidae), in Brazil. Braz J Biol 73 (in press)Google Scholar
  32. Matile-Ferrero D, Étienne J, Tiego G (2000) Introduction de deux ravageurs d’importance pour la Guyane française: Maconellicoccus hirsutus et Paracoccus marginatus (Hem., Coccoidea, Pseudococcidae). Bulletin de la Société Entomologique de France 105(5):485–486Google Scholar
  33. Meyerdirk DE, Warkentin R, Attavian B, Gersabeck E, Francis A, Adams J, Francis G (2001) Biological control of pink hibiscus mealybug project manual. USDA, Washington. http://www.aphis.usda.gov/import_export/plants/manuals/domestic/downloads/phm.pdf. Accessed 14 Sep 2012
  34. Michaud JP (2003) Three targets of classical biological control in the Caribbean: success, contribution, and failure. In: Van Dreische RG (ed) Proceedings of the first international symposium on biological control of arthropods. FHTET-03-05. USDA Forest Service Washington, pp 335–342Google Scholar
  35. Michaud JP, Evans GA (2000) Current status of pink hibiscus mealybug in Puerto Rico including a key to parasitoid species. Fla Entomol 83(1):97–101CrossRefGoogle Scholar
  36. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: current state and trends. Island Press, WashingtonGoogle Scholar
  37. Miller DR (1999) Identification of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Sternorrhyncha: Pseudococcidae). Insecta Mundi 13(3/4):189–202Google Scholar
  38. Ministério da Agricultura (2011) Roraima tem saída de mudas de vegetais proibida. http://www.agricultura.gov.br/vegetal/noticias/2011/08/roraima-tem-saida-de-mudas-de-vegetais-proibida. Accessed 13 Mar 2013
  39. Ministério da Agricultura (2013) Fitossanitárias. http://www.agricultura.gov.br/internacional/negociacoes/multilaterais/fitossanitarias. Accessed 13 Mar 2013
  40. Nalini T, Manickavasagam S (2011) Records of Encyrtidae (Hymenoptera: Chalcidoidea) parasitoids on mealybugs (Hemiptera: Pseudococcidae) from Tamil Nadu. India Check List 7:510–515Google Scholar
  41. Noyes JS (2012) Universal Chalcidoidea Database. World Wide Web electronic publication. http://www.nhm.ac.uk/chalcidoids Accessed 14 Sep 2012
  42. OEPP/EPPO (2005) Data sheets on quarantine pests Maconellicoccus hirsutus. Bull OEPP/EPPO Bull 35:413-415Google Scholar
  43. OEPP/EPPO (2006) Diagnostics Maconellicoccus hirsutus. Bull OEPP/EPPO Bull 36:167–169Google Scholar
  44. OIRSA (2012) Programa de control biológico de la cochinilla rosada. OIRSA (Organismo Internacional Regional de Sanidad Agropecuaria. http://www.oirsa.org/portal/CochinillaRosada.aspx. Accessed 5 Nov 2012
  45. Parra JRP, de Oliveira HN, de PintoA S (2003) Guia ilustrado de pragas e insetos benéficos dos citros. A de S Pinto, PiracicabaGoogle Scholar
  46. Radosevich S (2007) Plant invasions and their management. In: CIPM (ed) Invasive plant management: CIPM online textbook. Center for Invasive Plant Management, Bozeman. http://www.weedcenter.org/textbook/3_rados_invasion.html. Accessed 14 Mar 2013
  47. Ramos PEE, Hernández HG (2010) Plan de contingencia ante un brote de cochinilla rosada del hibisco (Maconellicoccus hirsutus) en un país de la región del OIRSA. OIRSA, San SalvadorGoogle Scholar
  48. Reddy GVP, Muniappan R, Cruz ZT, Naz F, Bamba JP, Tenorio J (2009) Present status of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in the Mariana Islands and its control by two fortuitously introduced natural enemies. J Econ Entomol 102(4):1431–1439PubMedCrossRefGoogle Scholar
  49. Roltsch WJ, Meyerdirk DE, Warkentin R, Andress ER, Carrera K (2006) Classical biological control of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green), in southern California. Biol Control 37(2):155–166CrossRefGoogle Scholar
  50. Rung A, Venable GL, Miller DR, Gill RJ, Williams DJ (2007) Scale insects: identification tools for species of quarantine importance. Scale Families. USDA, Washington. http://www.sel.barc.usda.gov/ScaleKeys/Mealybugs/Key/Mealybugs/Media/html/AboutFset.html. Accessed 14 Sep 2012
  51. Sagarra LA, Peterkin DD (1999) Invasion of the Caribbean by the hibiscus mealybug, Maconellicoccus hirsutus Green (Homoptera: Pseudococcidae). Phytoprotection 80(2):103–113CrossRefGoogle Scholar
  52. Sanches NF, Carvalho R da S (2010) Procedimentos para manejo da criação e multiplicação do predador exótico Cryptolaemus montrouzieri, Circular Técnica 99. Embrapa Mandioca e Fruticultura, Cruz das AlmasGoogle Scholar
  53. Sanches NF, Carvalho R da S, Silva ES, Santos IP, Caldas RC (2002) Técnica de criação do predador exótico Cryptolaemus montrouzieri Mulsant (Col.; Coccinellidae) em laboratório, Circular Técnica 47. Embrapa Mandioca e Fruticultura, Cruz das AlmasGoogle Scholar
  54. Schrader G, Unger JG (2003) Plant quarantine as a measure against invasive alien species: the framework of the International Plant Protection Convention and the plant health regulations in the European Union. Biol Invasions 5:357–364CrossRefGoogle Scholar
  55. Serrano MS, Lapointe SL (2002) Evaluation of host plants and a meridic diet for rearing Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) and its parasitoid Anagyrus kamali (Hymenoptera : Encyrtidae). Fla Entomol 85(3):417–425CrossRefGoogle Scholar
  56. Simberloff D (2009) We can eliminate invasions or live with them. Successful management projects Biol Invasions 11:149–157CrossRefGoogle Scholar
  57. SINAVEF (2010) Reporte epidemiológico cochinilla rosada del hibisco. SINAVEF, San Luis Potosí. http://portal.sinavef.gob.mx/documentos/BoletinesVarios/4_2_5RE_CRH001.pdf. Accessed 9 Nov 2012
  58. Singh SP (2004) Some success stories in classical biological control of agricultural pests in India. APAARI Publ 2004/2, Asia-Pacific association of agricultural research institutions, BangkokGoogle Scholar
  59. Tambasco FJ, Sá LAN, de Nardo EAB, Tavares MT (2000) Cochonilha rosada, Maconellicoccus hirsutus (Green): uma praga de importancia quarentenaria ja se encontra na guiana inglesa. Floresta 30(1–2):85–93Google Scholar
  60. Venette RC, Carey JR (1998) Invasion biology: rethinking our response to alien species. Calif Agric 52:13–17CrossRefGoogle Scholar
  61. Vitullo J, Zhang A, Mannion C, Bergh JC (2009) Expression of feeding symptoms from pink hibiscus mealybug (Hemiptera: Pseudococcidae) by commercially important cultivars of hibiscus. Fla Entomol 92:248–254CrossRefGoogle Scholar
  62. Williams DJ (1996) A brief account of the hibiscus mealybug Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), a pest of agriculture and horticulture, with descriptions of two related species from southern Asia. Bull Entomol Res 86:617–628CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Mark P. Culik
    • 1
  • Maurício José Fornazier
    • 1
    • 2
  • David dos Santos Martins
    • 1
  • José Salazar ZanuncioJr.
    • 1
  • José Aires Ventura
    • 1
  • Ana Lúcia B. G. Peronti
    • 3
  • José Cola Zanuncio
    • 2
  1. 1.Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural–INCAPERVitóriaBrazil
  2. 2.Departamento de EntomologiaUniversidade Federal de Viçosa–UFVViçosaBrazil
  3. 3.Departamento de Ecologia e Biologia EvolutivaUniversidade Federal de São Carlos–UFSCarSão CarlosBrazil

Personalised recommendations