Functional response of the mirid predators Dicyphus bolivari and Dicyphus errans and their efficacy as biological control agents of Tuta absoluta on tomato

  • B. L. IngegnoEmail author
  • G. J. Messelink
  • N. Bodino
  • A. Iliadou
  • L. Driss
  • J. B. Woelke
  • A. Leman
  • L. Tavella
Original Paper


Dicyphus bolivari Lindberg and Dicyphus errans (Wolff) (Hemiptera: Miridae) are naturally widespread in many crops with low-pesticide pressure, where they prey upon several arthropods, including the tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). However, their efficacy as biological control agents (BCAs) of this pest needs further investigations. Therefore, in this study the predatory efficacy of D. bolivari and of D. errans on T. absoluta was evaluated on tomato in laboratory and greenhouse trials. Their functional response to different numbers of T. absoluta eggs (up to 350) offered to single females or 5th-instar nymphs for 24 h was assessed in laboratory. Females and nymphs of both predators showed a high voracity and a type II functional response, with an estimated maximum predation rate per day of 189 and 194 eggs for D. bolivari females and nymphs, respectively, and 197 and 179 eggs for D. errans females and nymphs, respectively. The predators showed similar predation rates of T. absoluta eggs on plants in cage trials. However, our greenhouse trial showed that the commonly used Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae), which has a lower individual predation capacity than D. bolivari and D. errans, was more effective in controlling T. absoluta than D. errans and D. bolivari because of its stronger numerical response to densities of T. absoluta and supplemental food than the other two predator species. This shows that long-term greenhouse trials, which include functional and numerical responses to pest densities, are essential to evaluate the efficacy of an omnivorous predator.


Hemiptera: Miridae Lepidoptera: Gelechiidae South American tomato pinworm Numerical response Predator voracity 



The functional response and predation cage trials were partly supported by the Italian national project “Insects and globalization: sustainable control of exotic species in agro-forestry ecosystems (GEISCA)” of the Italian Ministry of University and Research. The greenhouse trial of Wageningen University & Research was funded by the Dutch top sector Horticulture and Starting Materials. The research was partly carried out during a Short Term Scientific Mission of COST Action FA1105 “Towards a sustainable and productive EU organic greenhouse horticulture”.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abbas S, Pérez-Hedo M, Colazza S, Urbaneja A (2014) The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. BioControl 59:565–574. CrossRefGoogle Scholar
  2. Abrams PA (1982) Functional responses of optimal foragers. Am Nat 120:382–390. CrossRefGoogle Scholar
  3. Alvarado P, Baltà O, Alomar O (1997) Efficiency of four Heteroptera as predators of Aphis gossypii and Macrosiphum euphorbiae (Hom.: Aphididae). Entomophaga 42:215–226. CrossRefGoogle Scholar
  4. Biondi A, Zappalà L, Di Mauro A, Tropea Garzia G, Russo A, Desneux N, Siscaro G (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? BioControl 61(1):79–90. CrossRefGoogle Scholar
  5. Biondi A, Guedes RNC, Wan F-H, Desneux N (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. CrossRefGoogle Scholar
  6. Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton, pp 351–356 (ISBN 0691125228)Google Scholar
  7. Briggs CJ, Hoopes MF (2004) Stabilizing effects in spatial parasitoid–host and predator–prey models: a review. Theor Popul Biol 65:299–315. CrossRefGoogle Scholar
  8. Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the Western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci 90:787–796. CrossRefGoogle Scholar
  9. Castañé C, Arnó J, Gabarra R, Alomar Ò (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29. CrossRefGoogle Scholar
  10. Coll M, Ridgway RL (1995) Functional and numerical responses of Orius insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops. Ann Entomol Soc Am 88:732–738. CrossRefGoogle Scholar
  11. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narvaez-Vasquez CA, Gonzalez-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, 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. CrossRefGoogle Scholar
  12. Enkegaard A, Brødsgaard HF, Hansen DL (2001) Macrolophus caliginosus: functional response to whiteflies and preference and switching capacity between whiteflies and spider mites. Entomol Exp Appl 101:81–88. CrossRefGoogle Scholar
  13. Fantinou AA, Perdikis DC, Maselou DA, Lambropoulos PD (2008) Prey killing without consumption: Does Macrolophus pygmaeus show adaptive foraging behaviour? Biol Control 47:187–193. CrossRefGoogle Scholar
  14. Fellowes MDE, Van Alphen JJM, Jervis MA (2007) Foraging Behaviour. In: Jervis MA (ed) Insects as natural enemies. A practical perspective. Springer Netherlands, Amsterdam, pp 1–72 (ISBN 978-1-4020-2625-6)Google Scholar
  15. Fernández-Arhex V, Corley JC (2003) The functional response of parasitoids and its implications for biological control. Biocontrol Sci Technol 13:403–413. CrossRefGoogle Scholar
  16. Ferracini C, Bueno VHP, Dindo ML, Ingegno BL, Luna MG, Salas Gervassio NG, Sánchez NE, Siscaro G, van Lenteren JC, Zappalà L, Tavella L (2019) Natural enemies of Tuta absoluta in the Mediterranean basin. Biocont Sci Technol Eur S Am. Google Scholar
  17. Foglar H, Malausa JC, Wajnberg E (1990) The functional response and preference of Macrolophus caliginosus [Heteroptera: Miridae] for two of its prey: Myzus persicae and Tetranychus urticae. Entomophaga 35:465–474. CrossRefGoogle Scholar
  18. Haddaway NR, Wilcox RH, Heptonstall REA, Griffiths HM, Mortimer RJG, Christmas M, Dunn AM (2012) Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS ONE 7:e32229. CrossRefGoogle Scholar
  19. Hamdan A-JS (2006) Functional and numerical responses of the predatory bug Macrolophus caliginosus Wagner fed on different densities of eggs of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood). J Biol Res 6:147–154Google Scholar
  20. Hassell MP (2000) Host–parasitoid population dynamics. J Anim Ecol 69:543–566. CrossRefGoogle Scholar
  21. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229. CrossRefGoogle Scholar
  22. Ingegno BL, Goula M, Navone P, Tavella L (2008) Distribution and host plants of the genus Dicyphus in the Alpine valleys of NW Italy. Bull Insectol 61:139–140 (ISSN 1721-8861)Google Scholar
  23. 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. CrossRefGoogle Scholar
  24. Ingegno BL, Candian V, Psomadelis I, Bodino N, Tavella L (2017a) The potential of host plants for biological control of Tuta absoluta by the predator Dicyphus errans. Bull Entomol Res 107:340–348. CrossRefGoogle Scholar
  25. Ingegno BL, Bodino N, Leman A et al (2017b) Predatory efficacy of Dicyphus errans on different prey. Acta Hortic 1164:425–430. CrossRefGoogle Scholar
  26. 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:e82231. CrossRefGoogle Scholar
  27. Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves, p. 159–182. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Chapman and Hall, New York, p 373Google Scholar
  28. Koller M, Knapp M, Schausberger P (2007) Direct and indirect adverse effects of tomato on the predatory mite Neoseiulus californicus feeding on the spider mite Tetranychus evansi. Entomol Exp Appl 125:297–305. CrossRefGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. Leman A, Ingegno BL, Tavella L, Janssen A, Messelink GJ (2019) The omnivorous predator Macrolophus pygmaeus, a good candidate for the control of both greenhouse whitefly and poinsettia thrips on gerbera plants. Insect Sci. Google Scholar
  31. Maselou DA, Perdikis DC, Sabelis MW, Fantinou AA (2014) Use of plant resources by an omnivorous predator and the consequences for effective predation. Biol Control 79:92–100. CrossRefGoogle Scholar
  32. Maselou DA, Perdikis DC, Fantinou A (2015) Effect of hunger level on prey consumption and functional response of the predator Macrolophus pygmaeus. Bull Insectol 68:211–218 (ISSN 1721-8861)Google Scholar
  33. Messelink GJ, Bennison J, Alomar O, Ingegno BL, Tavella L, Shipp L, Palevsky E, Wäckers FL (2014) Approaches to conserving natural enemy populations in greenhouse crops: current methods and future prospects. BioControl 59:377–393. CrossRefGoogle Scholar
  34. Michaelides G, Sfenthourakis S, Pitsillou Seraphides N (2018) Functional response and multiple predator effects of two generalist predators preying on Tuta absoluta eggs. Pest Manag Sci 74:332–339. CrossRefGoogle Scholar
  35. Montserrat M, Albajes R, Castañé C (2000) Functional response of four Heteropteran predators preying on greenhouse whitefly (Homoptera: Aleyrodidae) and western flower thrips (Thysanoptera: Thripidae). Environ Entomol 29:1075–1082. CrossRefGoogle Scholar
  36. Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39:335–354. CrossRefGoogle Scholar
  37. Nachman G (2006) A functional response model of a predator population foraging in a patchy habitat: functional response in a patchy environment. J Anim Ecol 75:948–958. CrossRefGoogle Scholar
  38. Okuyama T (2012a) On selection of functional response models: Holling’s models and more. BioControl 58:293–298. CrossRefGoogle Scholar
  39. Okuyama T (2012b) A likelihood approach for functional response models. Biol Control 60:103–107CrossRefGoogle Scholar
  40. Pereyra PC, Sánchez NE (2006) Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 35:671–676. CrossRefGoogle Scholar
  41. R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (ISBN: 3-900051-07-0)Google Scholar
  42. Roditakis E, Vasakis E, García-Vidal L, del Rosario Martínez-Aguirre M, Rison JL, Haxaire-Lutun MO, Nauen R, Tsagkarakou A, Bielza P (2018) A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. J Pest Sci 91:421–435. CrossRefGoogle Scholar
  43. Sanchez JA, Cassis G (2018) Towards solving the taxonomic impasse of the biocontrol plant bug subgenus Dicyphus (Dicyphus) (Insecta: Heteroptera: Miridae) using molecular, morphometric and morphological partitions. Zool J Linn Soc. (epub ahead of print)
  44. Tropea Garzia G, Siscaro G, Biondi A, Zappalà L (2012) Tuta absoluta, a South American pest of tomato now in the EPPO region: biology, distribution and damage. EPPO Bull 42:205–210. CrossRefGoogle Scholar
  45. Urbaneja A, Monton 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. CrossRefGoogle Scholar
  46. Van Den Meiracker RAF, Sabelis MW (1999) Do functional responses of predatory arthropods reach a plateau? A case study of Orius insidiosus with western flower thrips as prey. Entomol Exp Appl 90:323–329. CrossRefGoogle Scholar
  47. Van Lenteren JH, Hemerik L, Lins JC Jr, Bueno VHP (2016) Functional responses of three neotropical mirid predators to eggs of Tuta absoluta on tomato. Insects 7:34. CrossRefGoogle Scholar
  48. Voigt D, Gorb E, Gorb S (2007) Plant surface–bug interactions: Dicyphus errans stalking along trichomes. Arthropod-Plant Interact 1:221–243. CrossRefGoogle Scholar
  49. Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò 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(4):635–647. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), ULF Entomologia Generale e ApplicataUniversity of TorinoGrugliascoItaly
  2. 2.Business Unit Greenhouse HorticultureWageningen University & ResearchBleiswijkThe Netherlands

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