Skip to main content
Log in

Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis?

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is an important natural enemy of several key arthropod pests. However, in tomato crop this predator can cause economic damage owing to its zoophytophagous behavior. We investigated in laboratory conditions the influence of two alternative plants, Dittrichia viscosa L. (Asteraceae) and Sesamum indicum (L.) (Pedaliaceae), with or without prey, on N. tenuis damage and its biological control services on Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) eggs. Both D. viscosa and S. indicum, as companion plants in dual-choice bioassays, significantly reduced the damage of the mirid on tomato. S. indicum was more attractive than D. viscosa for feeding and oviposition and its presence did not interfere with the predation on T. absoluta eggs. We also studied the potential of the three plants as preyless rearing substrate for the mirid, and only S. indicum showed to be a suitable host plant for N. tenuis development and oviposition. The potential applications of S. indicum in N. tenuis field management and mass rearing are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahirwar RM, Gupta MP, Banerjee S (2010) Field efficacy of natural and indigenous products on sucking pests of Sesame. Indian J Nat Prod Resour 1:221–226

    Google Scholar 

  • Arnó J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520

    Article  Google Scholar 

  • Arnó J, Castañé C, Riudavets J, Gabarra R (2010) Risk of damage to tomato crops by the generalist zoophytophagous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae). Bull Entomol Res 100:105–115

    Article  PubMed  Google Scholar 

  • Biondi A, Chailleux A, Lambion J, Han P, Zappalà L, Desneux N (2013a) Indigenous natural enemies attacking Tuta absoluta (Lepidoptera: Gelechiidae) in southern France. Egypt J Biol Pest Contr 23:117–121

    Google Scholar 

  • Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013b) Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the Neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 106:1638–1647

    Article  PubMed  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    Article  PubMed  CAS  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013c) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):e76548

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Biondi A, Zappalà L, Desneux N, Aparo A, Siscaro G, Rapisarda C, Martin T, Tropea Garzia G (2015) Potential toxicity of α-cypermethrin-treated net on Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 108:1191–1197

    Article  PubMed  CAS  Google Scholar 

  • Bompard A, Jaworski CC, Bearez P, Desneux N (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 FJ, Bolckmans K, Belda JE (2009) Development of a biological control based Integrated Pest Management method for Bemisia tabaci for protected sweet pepper crops. Entomol Exp Appl 133:9–18

    Article  CAS  Google Scholar 

  • Calvo FJ, Lorente MJ, Stansly PA, Belda JE (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, Silva TB, Silva WM, Silva JE, Siqueira HA (2015) Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 88:405–412

    Article  Google Scholar 

  • Cano M, Vila E, Janssen D, Bretones G, Salvador E, Lara L, Tellez M (2009) Selection of refuges for Nesidiocoris tenuis (Het.: Miridae) and Orius laevigatus (Het.: Anthocoridae): virus reservoir risk assessment. IOBC/WPRS Bull 49:281–286

    Google Scholar 

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

    Article  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013a) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541

    Article  Google Scholar 

  • Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013b) Suitability of the pest–plant system Tuta absoluta (Lepidoptera: Gelechiidae)–tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. J Econ Entomol 106:2310–2321

    Article  PubMed  Google Scholar 

  • Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297

    Article  PubMed  CAS  Google Scholar 

  • De Puysseleyr V, De Man S, Hofte M, De Clercq P (2013) Plantless rearing of the zoophytophagous bug Nesidiocoris tenuis. BioControl 58:205–213

    Article  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello C, Urbaneja A (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 

  • Gillespie DR, McGregor RR (2000) The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation. Ecol Entomol 25:380–386

    Article  Google Scholar 

  • Haddi K, Berger M, Bielza P, Cifuentes D, Field LM, Gorman K, Rapisarda C, Williamson MS, Bass C (2012) Identification of mutations associated with pyrethroid resistance in the voltage-gated sodium channel of the tomato leaf miner (Tuta absoluta). Insect Biochem Mol Biol 42:506–513

    Article  PubMed  CAS  Google Scholar 

  • Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252

    Article  Google Scholar 

  • Jaworski CC, Bompard A, Genies L, Amiens-Desneux E, Desneux N (2013) Preference and prey switching in a generalist predator attacking local and invasive alien pests. PLoS ONE 8(12):e82231

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee MS, Albajes R, Eizaguirre M (2014) Mating behaviour of female Tuta absoluta (Lepidoptera: Gelechiidae): polyandry increases reproductive output. J Pest Sci 87:429–439

    Article  Google Scholar 

  • Lin K, Lu Y, Wan P, Yang Y, Wyckhuys KA, Wu K (2015) Simultaneous reduction in incidence of Bemisia tabaci (Hemiptera: Aleyrodidae) and Sylepta derogata (Lepidoptera: Pyralidae) using velvetleaf, Abutilon theophrasti as a trap crop. J Pest Sci 88:49–56

    Article  Google Scholar 

  • Lykouressis D, Giatropoulos A, Perdikis D, Favas C (2008) Assessing the suitability of noncultivated plants and associated insect prey as food sources for the omnivorous predator Macrolophus pygmaeus (Hemiptera: Miridae). Biol Control 44:142–148

    Article  Google Scholar 

  • Lykouressis D, Perdikis D, Charalampous P (2014) Plant food effects on prey consumption by the omnivorous predator Macrolophus pygmaeus. Phytoparasitica 42:303–309

    Article  Google Scholar 

  • Mbabie B, Omosun G, Uti A, Oyedemi S (2010) Chemical composition of Sesamum indicum L. (Sesame) grown in Southeastern Nigeria and the physicochemical properties of the seed oil. Seed Sci Biotech 4:69–72

    Google Scholar 

  • Messelink GJ, Bennison J, Alomar O, Ingegno BL, Tavella L, Shipp L, Palevsky E, Wäckers L (2014) Approaches to conserving natural enemy populations in greenhouse crops: current methods and future prospects. BioControl 54:377–393

    Article  Google Scholar 

  • Mollá O, González-Cabrera J, Urbaneja A (2011) The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. BioControl 56:883–891

    Article  Google Scholar 

  • Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (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, Gabarra R, Symondson WOC, King RA, Agustí N (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 

  • Nakaishi K, Fukui Y, Arakawa R (2011) Reproduction of Nesidiocoris tenuis (Reuter) on Sesame. J Appl Entomol Zool 55:199–205

    Article  Google Scholar 

  • Parolin P, Bresch C, Poncet C, Desneux N (2014) Introducing the term ‘Biocontrol Plants’ for integrated pest management. Sci Agric 71:77–80

    Article  Google Scholar 

  • Perdikis D, Favas C, Lykouressis D, Fantinou A (2007) Ecological relationships between non-cultivated plants and insect predators in agroecosystems: the case of Dittrichia viscosa (Asteraceae) and Macrolophus melanotoma (Hemiptera: Miridae). Acta Oecol 31:299–306

    Article  Google Scholar 

  • Perdikis D, Fantinou A, Lykouressis D (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biol Control 59:13–21

    Article  Google Scholar 

  • Pérez-Hedo M, Urbaneja A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73

    Article  Google Scholar 

  • Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Flors V, Urbaneja A (2015) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88:543–554

    Article  Google Scholar 

  • Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

    Article  PubMed  CAS  Google Scholar 

  • Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88:9–16

    Article  Google Scholar 

  • Rodriguez-Saona C, Crafts-Brandner SJ, Williams L III, Parè PW (2002) Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants. J Chem Ecol 28:1733–1747

    Article  PubMed  CAS  Google Scholar 

  • Rosenheim JA, Goeriz RE, Thacher EF (2004) Omnivore or herbivore? Field observations of foraging by Lygus hesperus (Hemiptera: Miridae). Environ Entomol 33:1362–1370

    Article  Google Scholar 

  • Saeed R, Razaq M, Hardy IC (2015) The importance of alternative host plants as reservoirs of the cotton leaf hopper, Amrasca devastans, and its natural enemies. J Pest Sci 88:517–531

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

    Article  PubMed  CAS  Google Scholar 

  • Sanchez JA, La Spina M, Lacasa A (2014) Numerical response of Nesidiocoris tenuis (Hemiptera: Miridae) preying on Tuta absoluta (Lepidoptera: Gelechiidae) in tomato crops. Eur J Entomol 111:387–395

    Article  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  PubMed  CAS  Google Scholar 

  • Tedeschi R, Alma A, Tavella L (2001) Side-effects of three neem (Azadirachta indica A. Juss) products on the predator Macrolophus caliginosus Wagner (Het., Miridae). J Appl Entomol 125:397–402

    Article  CAS  Google Scholar 

  • Urbaneja A, Tapia G, Stansly P (2005) Influence of host plant and prey availability on developmental time and survivorship of Nesidiocoris tenius (Het.: Miridae). Biocontrol Sci Technol 15:513–518

    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-Bernat P, Mollá O, Alonso M, Bolkcmans K, Urbaneja A, Tena A (2015) Sugars as complementary alternative food for the establishment of Nesidiocoris tenuis in greenhouse tomato. J Appl Entomol 139:161–167

    Article  CAS  Google Scholar 

  • Vacante V, Tropea Garzia G (1994) Nesidiocoris tenuis: antagonista naturale di aleurodidi. Informatore fitopatologico 4:23–28

    Google Scholar 

  • Vandekerkhove B, De Clercq P (2010) Pollen as an alternative or supplementary food for the mirid predator Macrolophus pygmaeus. Biol Control 53:238–242

    Article  Google Scholar 

  • Velasco-Hernández MC, Ramirez-Romero R, Sánchez-Hernández C, Biondi A, Muñoz-Urias A, Desneux N (2015) Foraging behavior of the parasitoid Eretmocerus eremicus under intraguild predation risk by Macrolophus pygmaeus. Pest Manag Sci 71:1346–1353

    Article  PubMed  Google Scholar 

  • Zappalà L, Siscaro G, Biondi A, Mollá O, Gonzalez-Cabrera J, Urbaneja A (2012a) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136:401–409

    Article  Google Scholar 

  • Zappalà L, Bernardo U, Biondi A, Cocco A, Deliperi S, Delrio G, Giorgini M, Pedata P, Rapisarda C, Tropea Garzia G, Siscaro G (2012b) Recruitment of native parasitoids by the exotic pest Tuta absoluta (Meyrick) in Southern Italy. Bull Insectol 65:51–61

    Google Scholar 

  • Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnó J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Vercher Aznar R, Urbaneja A, Desneux N (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 

  • Zhang X, Xu Q, Lu W, Liu F (2015) Sublethal effects of four synthetic insecticides on the generalist predator Cyrtorhinus lividipennis. J Pest Sci 88:383–392

    Article  Google Scholar 

  • Zhu P, Gurr GM, Lu Z, Heong K, Chen G, Zheng X, Xu H, Yang Y (2013) Laboratory screening supports the selection of sesame (Sesamum indicum) to enhance Anagrus spp. parasitoids (Hymenoptera: Mymaridae) of rice planthoppers. Biol Control 64:83–89

    Article  Google Scholar 

  • Zhu P, Lu Z, Heong K, Chen G, Zheng X, Zhu XuH, Yang Y, Nicol HI, Gurr GM (2014) Selection of nectar plants for use in ecological engineering to promote biological control of rice pests by the predatory bug, Cyrtorhinus lividipennis, (Heteroptera: Miridae). PLoS ONE 9(9):e108669

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank two anonymous referees, the handling editor and the editor-in-chief for the very helpful comments on the earlier versions of the manuscript. This research was partially funded by the Italian Ministry of Education, University and Research (PRIN project GEISCA, 2010CXXHJE_004), and by the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme FP7/2007-2013 under REA grant agreement n° 318246.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gaetano Siscaro.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Josep Anton Jaques Miret.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Biondi, A., Zappalà, L., Di Mauro, A. et al. Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis?. BioControl 61, 79–90 (2016). https://doi.org/10.1007/s10526-015-9700-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-015-9700-5

Keywords

Navigation