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Supplemental releases of specialist parasitic wasps improve whitefly and psyllid control by Dicyphus hesperus in tomato

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Abstract

Dicyphus hesperus Knight (Heteroptera: Miridae) can contribute to the suppression of populations of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and Bactericera cockerelli Sulcer (Hemiptera: Psyllidae) in tomato. Nevertheless, the remaining levels of these pests could still be too high for the crop to tolerate. We thus tested here whether the combination of D. hesperus with the specialist parasitoids Eretmocerus eremicus Rose & Zolnerowich (Hymenoptera: Aphelinidae) (whitefly) and Tamarixia triozae (psyllid) can result in better pest control compared with methods based exclusively on single-species releases in tomato. We conducted two simultaneous experiments in tomato (‘Whitefly’ and ‘Psyllid’ Experiment), where we compared the effectiveness against B. tabaci and B. cockerelli in cages receiving releases of the predator or the specialist parasitoid alone, or in combination. Although all natural enemies reduced pest levels when released separately, the combination of D. hesperus with E. eremicus and D. hesperus with T. triozae resulted in better whitefly and psyllid control, respectively, compared with the separate releases.

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References

  • Abbott WA (1925) A method to computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Banks E (2012) Potato zebra chip disease: a potential threat to processing & fresh market crop. Hortic Matters 13(10):6–7

    Google Scholar 

  • Bao-Fundadora L, Ramírez-Romero R, Sánchez-Hernández CV, Sánchez-Martínez J, Desneux N (2015) Intraguild predation of Geocoris punctipes on Eretmocerus eremicus and its influence on the control of the whitefly Trialeurodes vaporariorum. Pest Manag Sci 72:1110–1116

    Article  CAS  Google Scholar 

  • Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pest Biochem Physiol 121:78–87

    Article  CAS  Google Scholar 

  • Butler CD, Trumble JT (2012a) The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) life history, relationship to plant diseases, and management strategies. Terrest Arthropod Rev 5:87–111

    Article  Google Scholar 

  • Butler CD, Trumble JT (2012b) Identification and impact of natural enemies of Bactericera cockerelli (Hemiptera: Triozidae) in Southern California. J Econ Entomol 105:1509–1519

    Article  PubMed  Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2009) Development of a biological control-based IPM method for Bemisia tabaci for protected sweet pepper crops. Entomol Exp App 133:9–18

    Article  CAS  Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2012a) Release rate for a pre-plant application of Nesidiocoris tenuis for Bemisia tabaci control in tomato. BioControl 57:809–817

    Article  Google Scholar 

  • Calvo FJ, Lorente MJ, Stansly PA, Belda JE (2012b) Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisa tabaci in greenhouse tomato. Entomol Exp App 143:111–119

    Article  Google Scholar 

  • Calvo FJ, Torres-Ruiz A, Velázquez-González JC, Rodriguez-Leyva E, Lomeli-Flores JR (2016) Evaluation of Dicyphus hesperus for biological control of sweetpotato whitefly and potato psyllid on greenhouse tomato. BioControl 61:415–424

    Article  Google Scholar 

  • Calvo FJ, Torres A, González EJ, Velázquez MB (2018) The potential of Dicyphus hesperus as a biological control agent of potato psyllid and sweetpotato whitefly in tomato. Bull Entomol Res. https://doi.org/10.1017/S0007485318000020

    Article  PubMed  Google Scholar 

  • Cerón-González C, Lomeli-Flores JR, Rodríguez-Leyva E, Torres-Ruíz A (2014) Fertility and feeding of Tamarixia triozae (Hymenoptera: Eulophidae) on potato psyllid Bactericera cockerelli. Revista Mexicana de Ciencias Agrícolas 5:893–899

    Article  Google Scholar 

  • Cock MJW (1993) Bemisia tabaci: an update 1986–1992 on the cotton whitefly with an annotated bibliography. FAO Publishing. CAB International Institute of Biological Control, Ascot

    Google Scholar 

  • Colfer RG, Rosenheim JA (2001) Predation on immature parasitoids and its impact on prey suppression. Oecologia 126:292–304

    Article  PubMed  CAS  Google Scholar 

  • Cranshaw WS (1994) The potato (tomato) psyllid, Paratrioza cockerelli (Sulc), as a pest of potatoes. In: Zehnder GW, Powelson RK, Jansson RK, Raman KW (eds) Advances in potato biology and management. APS Press, St. Paul, pp 83–95

    Google Scholar 

  • Crawley MJ (2002) Statistical computing. An introduction to data analysis using S-plus. Wiley, Chichester

    Google Scholar 

  • Garzón-Tiznado JA, Cárdenas-Valenzuela OG, Bujanos-Muñiz R, Marín-Jarillo A (2009) Association of Hemiptera: Triozidae with the disease ‘‘permanente del tomate’’ in Mexico. Agricultura Técnica en México 35:61–72

    Google Scholar 

  • Gillespie DR, McGregor RR, Sánchez JA (2007) Dicyphus hesperus (Hemiptera: Miridae) as a success story in development of endemic natural enemies as biological control agents. In: Vincent CM, Goettel M, Lazarovits G (eds) Case studies in biological control: a global perspective. CABI Publishing, Oxfordshire, pp 128–135

    Chapter  Google Scholar 

  • Greenberg SM, Jones WA, Liu TX (2002) Interactions among two species of Eretmocerus (Hymenoptera: Aphelinidae), two species of whiteflies (Homoptera: Aleyrodidae), and tomato. Biol Control 31(2):397–402

    Google Scholar 

  • Headrick DH, Bellows TS, Perring TM (1999) Development and reproduction of a population of Eretmocerus eremicus (Hymenoptera: Aphelinidae) on Bemisia argentifolii (Homoptera: Aleyrodidae). Environ Entomol 28(2):300–306

    Article  Google Scholar 

  • Heinz KM, Nelson JM (1996) Interspecific interactions among natural enemies of Bemisia in an inundative biological control program. Biol Control 6:384–393

    Article  Google Scholar 

  • Hoddle MS, van Driesche RG (1999) Evaluation of Eretmocerus eremicus and Encarsia formosa (Hymenoptera: Aphelinidae) Beltsville strain in commercial greenhouses for biological control of Bemisia argentifolii (Homoptera: Aleyrodidae) on colored poinsettia plants. Florida Entomol 82:556–569

    Article  Google Scholar 

  • Jones RD (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219

    Article  Google Scholar 

  • McGregor RR, Gillespie DR (2005) Intraguild predation by the generalist predator Dicyphus hesperus on the parasitoid Encarsia formosa. Biocontrol Sci Techol 15(3):219–227

    Article  Google Scholar 

  • McGregor R, Gillespie D, Quiring D, Foisy M (1999) Potential use of Dicyphus hesperus Knight (Heteroptera: Miridae) for biological control of pests of greenhouse tomatoes. Biol Control 16:104–110

    Article  Google Scholar 

  • Messelink GJ, van Maanen R, van Steenpaal SEF, Janssen A (2008) Biological control of thrips and whiteflies by a shared predator: two pests are better than one. Biol Control 44:372–379

    Article  Google Scholar 

  • Munyaneza JE, Crosslin JM, Upton JE (2007) Association of Bactericera cockerelli (Homoptera: Psyllidae) with “Zebra Chip”, a new potato disease in Southwestern United States and Mexico. J Econ Entomol 100:656–663

    Article  PubMed  CAS  Google Scholar 

  • Myers J, Charlene H, Kovacs E (1989) How many insect species are necessary for the biological control of insects? Environ Entomol 18(4):541–547

    Article  Google Scholar 

  • Nauen R, Denholm I (2005) Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Arch Insect Biochem Physiol 58:200–215

    Article  PubMed  CAS  Google Scholar 

  • Northfield TD, Crowder DW, Jabbour R, Snyder WE (2012) Natural enemy functional identity, trait-mediated interactions and biological control. In: Ohgushi T, Schmitz O, Holt RD (eds) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, New York, pp 450–465

    Chapter  Google Scholar 

  • Palumbo JC, Horowitz AR, Prabhaker N (2001) Insecticidal control and resistance management for Bemisia tabaci. Crop Protect 20:739–765

    Article  CAS  Google Scholar 

  • Pimentel D, Burgess M (2014) Environmental and economic costs of the application of pesticides primarily in the United States. In: Pimentel D, Peshin R (eds) Integrated pest management. Springer, Dordrecht, pp 47–71

    Chapter  Google Scholar 

  • Ramírez-Ahuja ML, Rodríguez-Leyva E, Lomeli-Flores JR, Torres-Ruíz A, Guzmán-Franco AW (2017) Evaluating combined use of a parasitoid and a zoophytophagous bug for biological control of the potato psyllid, Bactericera cockerelli. Biol Control 106:9–15

    Article  Google Scholar 

  • Rojas P, Rodríguez-Leyva E, Lomeli-Flores JR, Liu TX (2015) Biology and life history of Tamarixia triozae (Hymenoptera: Eulophidae), a parasitoid of Bactericera cockerelli (Hemiptera: Triozidae). BioControl 60:27–35

    Article  Google Scholar 

  • Rosenheim JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annu Rev Entomol 43:421–447

    Article  PubMed  CAS  Google Scholar 

  • Sánchez JA, Gillespie DR, McGregor RR (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomol Exp App 112:7–19

    Article  Google Scholar 

  • Secor GA, Rivera VV, Abad JA, Lee IM, Clover GRG, Liefting LW, Li X, de Boer SH (2009) Association of ‘Candidatus Liberibacter solanacearum’ with zebra chip disease of potato established by graft and psyllid transmission, electron microscopy, and PCR. Plant Dis 93(6):574–583

    Article  CAS  Google Scholar 

  • Shipp JL, Wang K (2006) Evaluation of Dicyphus hersperus (Heteroptera: Miridae) for biological control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomato. J Econ Entomol 99(2):414–420

    Article  PubMed  CAS  Google Scholar 

  • Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716

    Article  Google Scholar 

  • Stansly PA, Calvo FJ, Urbaneja A (2005) Release rates for control of Bemisia tabaci (Homoptera: Aleyrodidae) biotype “Q” with Eretmocerus mundus (Hymenoptera: Aphelinidae) in greenhouse tomato and pepper. Biol Cont 35:124–133

    Article  Google Scholar 

  • Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237

    Article  Google Scholar 

  • Vet LM, van Lenteren JC (1981) The parasite-host relationship between Encarsia formosa Gah. (Hymenoptera:Aphelinidae) and Trialeurodes vaporariorum (Westw.) (Homoptera: Aleyrodidae). A composition of three Encarsia spp. and one Eretmocerus sp. to estimate their potentialities in controlling whitefly on tomatoes in greenhouses with a low temperature regime. J App Entomol 91:327–348

    Google Scholar 

  • Workman PJ, Whiteman SA (2009) Importing Tamarixia triozae into containment in New Zealand. N Z Plant Protect Soc 62:136–144

    Google Scholar 

  • Yang XB, Campos-Figueroa M, Silva A, Henne DC (2015) Functional response, prey stage preference, and mutual interference of the Tamarixia triozae (Hymenoptera: Eulophidae) on tomato and bell pepper. J Econ Entomol 108:414–424

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Authors thank Elizabeth Julieta González-Jaime (R&D Koppert Mexico SA de CV) for technical assistance. The authors also thank anonymous reviewers for providing valuable and constructive remarks. Special thanks to Karen Girard (R&D, Koppert Biological Systems, UK) for reviewing the manuscript and provide valuable remarks. This work was partially supported by the National Council of Science and Technology (CONACYT) [Grant Number PEI-CONACYT-223073_2015].

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Authors and Affiliations

  1. R&D Department, Koppert España S.L., C/ Cobre, 22. Polígono Ind. Ciudad del Transporte, 04745, La Mojonera, Almería, Spain

    F. J. Calvo

  2. R&D Department, Koppert México SA de CV, Circuito el Marqués Norte 82, Parque Ind., El Marqués, Querétaro, Mexico

    J. C. Velázquez-González, M. B. Velásquez-González & A. Torres

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  1. F. J. Calvo
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  2. J. C. Velázquez-González
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  3. M. B. Velásquez-González
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  4. A. Torres
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Correspondence to F. J. Calvo.

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Handling Editor: Dirk Babendreier.

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Calvo, F.J., Velázquez-González, J.C., Velásquez-González, M.B. et al. Supplemental releases of specialist parasitic wasps improve whitefly and psyllid control by Dicyphus hesperus in tomato. BioControl 63, 629–639 (2018). https://doi.org/10.1007/s10526-018-9898-0

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  • DOI: https://doi.org/10.1007/s10526-018-9898-0

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