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Combining mirid predators to reduce crop damage and sustain biocontrol in multi-prey systems

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Abstract

With the invasion or local occurrence of Bemisia tabaci and Tuta absoluta in recent decades, they both have become two major insect pests of tomato crops in many countries. The biological control of these two pests through heteropteran predators, e.g., Nesidiocoris tenuis or Macrolophus pygmaeus, is a key pest management strategy. However, by contrast to M. pygmaeus, N. tenuis could usually cause plant damage and yield loss. The joint use of these two mirids for pest management has not been described yet, although it may be helpful in reducing the side effects of N. tenuis on crop (owing to competitive and/or agonistic interactions between the two species). In this study, we compared the abundance of predators and pests in treatments with N. tenuis and M. pygmaeus together versus N. tenuis alone and in the presence of B. tabaci only or B. tabaci and T. absoluta. We also measured necrotic rings and tomato flower production in these four treatments. We found that the joint use of both mirid predators together led to (1) a reduced overall mirid density and (2) a sustained biocontrol efficiency, when compared to the use of N. tenuis alone. In addition, plant feeding activities of mirids were significantly reduced when predators were used jointly (vs. N. tenuis alone). The applicability of zoophytophagous predators as biocontrol agents could be facilitated by simultaneously releasing two (or more) heteropteran predator species instead of a single one.

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  • 24 September 2022

    Article title has been updated in the original article

References

  • Alomar O, Riudavets J, Castañe C (2006) Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biol Control 36:154–162

    Article  Google Scholar 

  • Aparicio Y, Gabarra R, Arno J (2020) Interactions among Myzus persicae, predators and parasitoids may hamper biological control in Mediterranean peach orchards. Entomol Gen 40:217–228

    Article  Google Scholar 

  • Arnemann JA, Bevilaqua JG, Bernardi L et al (2019) Integrated management of tomato whitefly under greenhouse conditions. J Agr Sci 11:443–453

    Google Scholar 

  • Arnó J, Castañé C, Riudavets J et al (2010) Risk of damage to tomato crops by the generalist zoophytophagous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae). B Entomol Res 100:105

    Article  Google Scholar 

  • Becker C, Han P, Campos MR, Bearez P, Thomine E et al (2021) Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints. Sci Total Environ 793:148544

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Zappalà L, Di Mauro A et al (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? Biocontrol 61:79–90

    Article  Google Scholar 

  • Biondi A, Guedes RNC, Wan FH et al (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: Past, present, and future. Annu Rev Entomol 63:239–258. https://doi.org/10.1146/annurev-ento-031616-034933

    Article  CAS  PubMed  Google Scholar 

  • Bompard A, Jaworski CC, Bearez P et al (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55:433–440

    Article  Google Scholar 

  • Calvo J, Bolckmans K, Stansly PA et al (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. Biocontrol 54:237–246

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Campos MR, Béarez P, Amiens-Desneux E, Ponti L et al (2021) Thermal biology of Tuta absoluta: demographic parameters and facultative diapause. J Pest Sci 94:829–842

    Article  Google Scholar 

  • Castañé C, Arnó J, Gabarra R et al (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29

    Article  Google Scholar 

  • Chen X, Jaworski CC, Dai H, Liang YY, Guo XJ, Wang S, Zang LS, Desneux N (2022) Combining banker plants to achieve long-term pest control in multi-pest and multi-natural enemy cropping systems. J Pest Sci 95:685–697

    Article  Google Scholar 

  • Chinchilla-Ramírez M, Garzo E, Fereres A et al (2021) Plant feeding by Nesidiocoris tenuis: Quantifying its behavioral and mechanical components. Biol Control 152:104402

    Article  Google Scholar 

  • Damien M, Llopis S, Desneux N, van Baaren J, Le Lann C (2020) How does floral nectar quality affect life history strategies in parasitic wasps? Entomol Gen 40:147–156

    Article  Google Scholar 

  • De Barro PJ, Liu SS, Boykin LM et al (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19

    Article  PubMed  Google Scholar 

  • Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna MG, Guillemaud T et al (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Desneux N, Han P, Mansour R et al (2022) Integrated pest management of Tuta absoluta: practical implementations across different world regions. J Pest Sci 95:17–39

    Article  Google Scholar 

  • Gavkare O, Sharma PL (2017) Influence of temperature on development of Nesidiocoris tenuis (Reuiter) preying on Trialeurodes vaporariorum (Westwood) on tomato. Entomol News 127(230–241):212

    Google Scholar 

  • Guedes RNC, Roditakis E, Campos MR et al (2019) Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. J Pest Sci 92:1329–1342

    Article  Google Scholar 

  • Han P, Zhang Y-N, Lu Z-Z, Wang S, Ma D-Y et al (2018) Are we ready for the invasion of Tuta absoluta? unanswered key questions for elaborating an integrated Pest management package in Xinjiang, China. Entomol Gen 38:113–125

    Article  Google Scholar 

  • Han P, Bayram Y, Shaltiel-Harpaz L et al (2019) Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J Pest Sci 92:1317–1327

    Article  Google Scholar 

  • Han P, Becker C, Le Bot J, Larbat R, Lavoir AV, Desneux N (2020) Plant nutrient supply alters the magnitude of indirect interactions between insect herbivores: from foliar chemistry to community dynamics. J Ecol 108:1497–1510

    Article  CAS  Google Scholar 

  • Han P, Lavoir A-V, Rodriguez-Saona C et al (2022) Bottom-Up forces in agroecosystems and their potential impact on arthropod pest management. Annu Rev Entomol 67:239–259

    Article  PubMed  Google Scholar 

  • Horowitz AR, Ghanim M, Roditakis E et al (2020) Insecticide resistance and its management in Bemisia tabaci species. J Pest Sci 93:893–910

    Article  Google Scholar 

  • Ingels R, Bosmans L, Pekas A et al (2022) Preference and plant damage caused by Nesidiocoris tenuis on twenty-one commercial tomato cultivars. J Pest Sci. https://doi.org/10.1007/s10340-022-01530-3

    Article  Google Scholar 

  • Jaworski CC, Bompard A, Genies L et al (2013) Preference and prey switching in a generalist predator attacking local and invasive alien pests. PLoS ONE 8:e82231

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaworski CC, Chailleux A, Bearez P et al (2015) Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss. J Pest Sci 88:793–803

    Article  Google Scholar 

  • Konan KAJ, Monticelli LS, Ouali-N’goran S-WM et al (2021) Combination of generalist predators, Nesidiocoris tenuis and Macrolophus pygmaeus, with a companion plant, Sesamum indicum: What benefit for biological control of Tuta absoluta? PLoS ONE 16:e0257925. https://doi.org/10.1371/journal.pone.0257925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucas É, Rosenheim JA (2011) Influence of extraguild prey density on intraguild predation by heteropteran predators: a review of the evidence and a case study. Biol Control 59:61–67

    Article  Google Scholar 

  • Mansour R, Biondi A (2021) Releasing natural enemies and applying microbial and botanical pesticides for managing Tuta absoluta in the MENA region. Phytoparasitica 49:179–194

    Article  Google Scholar 

  • Mansour R, Brévault T, Chailleux A, Cherif A, Grissa-Lebdi K et al (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38:83–112

    Article  Google Scholar 

  • Menail AH, Boutefnouchet-Bouchema WF, Haddad N et al (2020) Effects of thiamethoxam and pinosad on the survival and hypopharyngeal glands of the African honey bee (Apis mellifera intermissa). Entomol Gen 40:207–215

    Article  Google Scholar 

  • Michaelides G, Sfenthourakis S, Pitsillou M et al (2018) Functional response and multiple predator effects of two generalist predators preying on Tuta absoluta eggs. Pest Manag Sci 74:332–339

    Article  CAS  PubMed  Google Scholar 

  • Mollá O, Biondi A, Alonso-Valiente M et al (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biocontrol 59:175–183

    Article  Google Scholar 

  • Moreno-Ripoll R, Agustí N, Berruezo R et al (2012) Conspecific and heterospecific interactions between two omnivorous predators on tomato. Biol Control 62:189–196

    Article  Google Scholar 

  • Moreno-Ripoll R, Gabarra R, Symondson WOC et al (2014) Do the interactions among natural enemies compromise the biological control of the whitefly Bemisia tabaci? J Pest Sci 87:133–141

    Article  Google Scholar 

  • Mouratidis A, Leman A, Poelman EH et al (2022) Dicyphus predatory bugs pre-established on tomato plants reduce Nesidiocoris tenuis population growth. J Pest Sci. https://doi.org/10.1007/s10340-022-01482-8

    Article  Google Scholar 

  • Mugerwa H, Colvin J, Alicai T et al (2021) Genetic diversity of whitefly (Bemisia spp.) on crop and uncultivated plants in Uganda: implications for the control of this devastating pest species complex in Africa. J Pest Sci 94:1307–1330

    Article  CAS  Google Scholar 

  • Perdikis D, Lucas E, Garantonakis N et al (2014) Intraguild predation and sublethal interactions between two zoophytophagous mirids, Macrolophus pygmaeus and Nesidiocoris tenuis. Biol Control 70:35–41

    Article  Google Scholar 

  • Pérez-Hedo M, Urbaneja A (2016) The zoophytophagous predator Nesidiocoris tenuis: A successful but controversial biocontrol agent in tomato crops. In: Horowitz AR, Ishaaya I (eds) Advances in Insect Control and Resistance Management. Springer International Publishing, Cham, pp 121–138

    Chapter  Google Scholar 

  • Pérez-Hedo M, Alonso-Valiente M, Vacas S, Gallego C, Rambla JL, Navarro-Llopis V et al (2021a) Eliciting tomato plant defenses by exposure to herbivore induced plant volatiles. Entomol Gen 41:209–218

    Article  Google Scholar 

  • Pérez-Hedo M, Riahi C, Urbaneja A (2021b) Use of zoophytophagous mirid bugs in horticultural crops: Current challenges and future perspectives. Pest Manag Sci 77:33–42

    Article  PubMed  Google Scholar 

  • Pérez-Valencia LI, Camorlinga-Cortés P, Carrillo-Arámbula LC, Palmeros-Suárez PA, Ramirez-Romero R (2019) Why can a predator increase its consumption of prey when it is released along with a parasitoid? Entomol Gen 39:205–219. https://doi.org/10.1127/entomologia/2019/0810

    Article  Google Scholar 

  • Perović DJ, Gámez-Virués S, Landis DA, Wäckers F, Gurr GM, Wratten SD, You MS, Desneux N (2018) Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol Rev 93:306–321

    Article  PubMed  Google Scholar 

  • R Core Team (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Ramos RS, Kumar L, Shabani F et al (2018) Mapping global risk levels of Bemisia tabaci in areas of suitability for open field tomato cultivation under current and future climates. PLoS ONE 13:e0198925

    Article  PubMed  PubMed Central  Google Scholar 

  • Ranjbar F, Michaud JP, Jalali MA et al (2020) Intraguild predation between two lady beetle predators is more sensitive to density than species of extraguild prey. Biocontrol 65:713–725

    Article  Google Scholar 

  • Ricupero M, Abbes K, Haddi K, Kurtulus A et al (2020) Combined thermal and insecticidal stresses on the generalist predator Macrolophus pygmaeus. Sci Tot Environ 729:138922

    Article  CAS  Google Scholar 

  • Sanchez JA (2009) Density thresholds for Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops. Biol Control 51:493–498

    Article  Google Scholar 

  • Sanchez JA, López-Gallego E, Pérez-Marcos M et al (2018) How safe is it to rely on Macrolophus pygmaeus (Hemiptera: Miridae) as a biocontrol agent in tomato crops? Front Ecol Evol 6:132

    Article  Google Scholar 

  • Sánchez JA, Lacasa A (2008) Impact of the zoophytophagous plant bug Nesidiocoris tenuis (Heteroptera: Miridae) on tomato yield. J Econ Entomol 101:1864–1870

    Article  PubMed  Google Scholar 

  • Sánchez-Hernández CV, Desneux N, Bao-Fundora L, Ramirez-Romero R (2021) Alternative extraguild prey modifies focal extraguild prey consumption and parasitism but not intraguild predation intensity. Biol Control 153:104475

    Article  Google Scholar 

  • Sharifian I, Sabahi Q, Khoshabi J (2015) Functional response of Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis (Reuter) feeding on two different prey species. Arch Phytopathol Plant Prot 48:910–920

    Article  Google Scholar 

  • Shen XN, Ji SX, Liu WX, Guo JY, Lu ZC, Wan FH (2021) Molecular characteristics of three cold resistance genes and their roles in temperature stress response in two Bemisia tabaci cryptic species. Entomol Gen 41:317–328

    Article  Google Scholar 

  • Soares MA, Campos MR, Passos LC, Carvalho GA et al (2019) Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta. J Pest Sci 92:1433–1443

    Article  Google Scholar 

  • Sylla S, Brevault T, Diarra K et al (2016) Life-history traits of Macrolophus pygmaeus with different prey foods. PLoS ONE 11:e0166610

    Article  PubMed  PubMed Central  Google Scholar 

  • Tadele S, Emana G (2018) Determination of the economic threshold level of tomato leaf miner, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) on tomato plant under glasshouse conditions. J Hortic for 10:9–16

    Article  Google Scholar 

  • Thomine E, Jeavons E, Rusch A, Bearez P, Desneux N (2020a) Effect of crop diversity on predation activity and population dynamics of the mirid predator Nesidiocoris tenuis. J Pest Sci 93:1255–1265

    Article  Google Scholar 

  • Thomine E, Rusch A, Supplisson C, Monticelli LS, Amiens-Desneux E, Lavoir AV, Desneux N (2020b) Highly diversified crop systems can promote the dispersal and foraging activity of the generalist predator Harmonia axyridis. Entomol Gen 40:133–145

    Article  Google Scholar 

  • Urbaneja A, Montón H, Mollá O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133:292–296

    Article  Google Scholar 

  • Urbaneja A, González-Cabrera J, Arnó J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68:1215–1222

    Article  CAS  PubMed  Google Scholar 

  • Wang MH, Ismoilov K, Li H, Zhang X, Lu ZZ, Feng LK et al (2021) Polygyny of Tuta absoluta may affect sex pheromone-based control techniques. Entomol Gen 41:357–367

    Article  Google Scholar 

  • Yao F-L, Zheng Y, Zhao J-W et al (2015) Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere 128:49–55

    Article  CAS  PubMed  Google Scholar 

  • Yao F-L, Zheng Y, Huang X-Y et al (2017) Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005–2014. Sci Rep 7:40803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zappala L, Biondi A, Alma A et al (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86:635–647

    Article  Google Scholar 

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Acknowledgements

This work was financially supported by the Oversea Study Scholarship and Young Scientists project (YC2015-2, CXTD2021004-3, XTCXGC2021011) of Fujian Academy of Agricultural Sciences to FLY and the project ACOR (Casdar) to ND.

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Authors and Affiliations

  1. State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Plant Protection, Fujian Academy of Agricultural Sciences, Fuzhou, 350013, China

    Feng-Luan Yao

  2. Fujian Key Laboratory for Monitoring and Integrated Management of Crop Pests, Fujian Engineering Research Center for Green Pest Management, Fuzhou, 350013, China

    Feng-Luan Yao

  3. Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000, Nice, France

    Feng-Luan Yao, Lucie S. Monticelli, Roger Boll, Kouassi A. J. Konan, Eva Thomine, Marica Scala, Philippe Bearez, Yanyan Qu & Nicolas Desneux

  4. Felix Houphouet Boigny University of Cocody, Abidjan, Côte d’Ivoire

    Kouassi A. J. Konan

  5. Center of Agriculture, Food & Environment (C3A), University of Trento, 38010, San Michele all’Adige, Italy

    Marica Scala

  6. Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

    Yanyan Qu

  7. Department of Agriculture, Food and Environment, University of Catania, 95123, Catania, Italy

    Antonio Biondi

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  1. Feng-Luan Yao
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  2. Lucie S. Monticelli
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  3. Roger Boll
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  9. Antonio Biondi
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  10. Nicolas Desneux
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Correspondence to Nicolas Desneux.

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Authors FLY, LSM, KAJK, YQ, MS, ET, PB and RB declare that they have no conflict of interest. Authors AB and ND are Editors-in-Chief of Journal of Pest Science and were not involved in the review process and decisions related to this manuscript.

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Yao, FL., Monticelli, L.S., Boll, R. et al. Combining mirid predators to reduce crop damage and sustain biocontrol in multi-prey systems. J Pest Sci 95, 1645–1657 (2022). https://doi.org/10.1007/s10340-022-01560-x

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