Journal of Plant Diseases and Protection

, Volume 124, Issue 3, pp 295–303 | Cite as

Inoculative release strategies of Macrolophus pygmaeus Rambur (Hemiptera: Miridae) in tomato crops: population dynamics and dispersal

  • Rob MoerkensEmail author
  • Els Berckmoes
  • Veerle Van Damme
  • Lieve Wittemans
  • Luc Tirry
  • Hans Casteels
  • Patrick De Clercq
  • Raf De Vis
Original Article


Macrolophus pygmaeus Rambur (Hemiptera: Miridae) is a key biological control agent in greenhouse tomato crops. In the present study, we describe the population dynamics of M. pygmaeus after release during two generations in semi-commercial greenhouses in order to optimize biocontrol programs. We tested the effect of the number of weekly supplementary food applications consisting of a mixture of Ephestia kuehniella Zeller and Artemia franciscana Kellogg in a tomato crop on population numbers of M. pygmaeus at low and high initial release densities of the predator. Also, the effect of supplementary feeding on the predator’s dispersal was studied. Larger population densities of M. pygmaeus were obtained when food was supplied for a longer period. However, we observed fruit damage by M. pygmaeus at high densities resulting from too frequent food applications. Also, dispersal was slowed down as the number of supplementary food applications increased. Distributing M. pygmaeus over more plants at release results in higher total population densities. The optimal inoculative release strategy of M. pygmaeus is a trade-off between high population densities and fruit damage, fast or slow dispersal throughout the greenhouse and the number of release plants and work/costs related to the supplementation of food. The optimal strategy to overcome negative effects like fruit damage, slow dispersal and potential cannibalism proved to be a weekly provision of supplementary food during 6–8 weeks, with an initial release density strategy of 20 M. pygmaeus adults per plant. These results contribute to a more sustainable tomato production. A reliable and efficient inoculative release strategy for the key predator M. pygmaeus enhances the biocontrol potential and is of great value for tomato growers.


Tomato Glasshouse vegetables Miridae Macrolophus pygmaeus Biocontrol Inoculative release strategy Population dynamics Dispersal 



The Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT) financed this study. The research Project 100888 was granted to Proefstation voor de Groenteteelt (R. De Vis and L. Wittemans) in cooperation with Proefcentrum Hoogstraten, Ghent University and the Institute for Agricultural and Fisheries Research.


  1. 1.
    Alomar, O., Riudavets, J., & Castañe, C. (2006). Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biological Control, 36, 154–162.CrossRefGoogle Scholar
  2. 2.
    Arnó, J., & Gabarra, R. (2011). Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). Journal of Pest Science, 84, 513–520.CrossRefGoogle Scholar
  3. 3.
    Blaeser, P., Sengonca, C., & Zegula, T. (2004). The potential use of different predatory bug species in the biological control of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Journal of Pest Science, 77, 211–219.CrossRefGoogle Scholar
  4. 4.
    Calvo, F. J., Lorente, M. J., Stansly, P. A., & Belda, J. E. (2012). Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisia tabaci in greenhouse tomato. Entomologia Experimentalis et Applicata, 143, 111–119.CrossRefGoogle Scholar
  5. 5.
    Castañé, C., Alomar, O., Goula, M., & Gabarra, R. (2004). Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biological Control, 30, 591–597.CrossRefGoogle Scholar
  6. 6.
    Enkegaard, A., Brodsgaard, H. F., & Hansen, D. L. (2001). Macrolophus caliginosus: Functional response to whiteflies and preference and switching capacity between whiteflies and spider mites. Entomologia Experimentalis et Applicata, 101, 81–88.CrossRefGoogle Scholar
  7. 7.
    De Clercq, P., Coudron, T. A., & Riddick, E. W. (2014). Production of heteropteran predators. In J. A. Morales-Ramos, G. Rojas, & D. Shapiro-Ilan (Eds.), Mass production of beneficial organisms: Invertebrates and entomopathogens (pp. 57–100). Amsterdam: Elsevier.CrossRefGoogle Scholar
  8. 8.
    Hamdi, F., Chadoeuf, J., & Bonato, O. (2013). Functional relationship between plant feeding and prey feeding for a zoophytophagous bug. Physiological Entomology, 38, 241–245.CrossRefGoogle Scholar
  9. 9.
    Hamdi, F., Chadoeuf, J., Chermiti, B., & Bonato, O. (2013). Evidence of cannibalism in Macrolophus pygmaeus, a natural enemy of whiteflies. Journal of Insect Behavior, 26, 614–621.CrossRefGoogle Scholar
  10. 10.
    Ingegno, B. I., Pansa, M. G., & Tavella, L. (2011). Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biological Control, 58, 174–181.CrossRefGoogle Scholar
  11. 11.
    Laycock, A., Camm, E., Van Laerhoven, S., & Gillespie, D. (2006). Cannibalism in a zoophytophagous omnivore is mediated by prey availability and plant substrate. Journal of Insect Behavior, 19, 219–229.CrossRefGoogle Scholar
  12. 12.
    Lenfant, C., Ridray, G., & Schoen, L. (2000). Biopropagation of Macrolophus caliginosus Wagner for a quicker establishment in Southern tomato greenhouses. IOBC/WPRS Bulletin, 23, 247–251.Google Scholar
  13. 13.
    Lykouressis, D. P., Perdikis, D., & Michalaki, M. (2001). Nymphal development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae) on two eggplant varieties as affected by temperature and presence/absence of prey. Biological Control, 20, 222–227.CrossRefGoogle Scholar
  14. 14.
    Lykouressis, D., Giatropoulos, A., Perdikis, D., & Favas, C. (2008). Assessing the suitability of non-cultivated plants and associated insect prey as food sources for the omnivorous predator Macrolophus pygmaeus (Hemiptera: Miridae). Biological Control, 44, 142–148.CrossRefGoogle Scholar
  15. 15.
    Moerkens, R., Berckmoes, E., Van Damme, V., Ortega-Parra, N., Hanssen, I., Wutack, M., et al. (2015). High population densities of Macrolophus pygmaeus on tomato plants can cause economic fruit damage: Interaction with Pepino mosaic virus? Pest Management Science, 72, 1350–1358.CrossRefPubMedGoogle Scholar
  16. 16.
    Moreno-Ripoll, R., Agustí, N., Berruezo, R., & Gabarra, R. (2012). Conspecific and heterospecific interactions between two omnivorous predators on tomato. Biological Control, 62, 189–196.CrossRefGoogle Scholar
  17. 17.
    Perdikis, D., & Lykouressis, D. (2000). Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biological Control, 17, 55–60.CrossRefGoogle Scholar
  18. 18.
    Perdikis, D., & Lykouressis, D. (2002). Life table and biological characteristics of Macrolophus pygmaeus when feeding on Myzus persicae and Trialeurodes vaporariorum. Entomologia Experimentalis et Applicata, 102, 261–272.CrossRefGoogle Scholar
  19. 19.
    Polis, G. A. (1981). The evolution and dynamics of intraspecific predation. Annual Review of Ecology and Systematics, 12, 225–251.CrossRefGoogle Scholar
  20. 20.
    Portillo, N., Alomar, O., & Wäckers, F. (2012). Nectarivory by the plant-tissue feeding predator Macrolophus pygmaeus Rambur (Heteroptera: Miridae): Nutritional redundancy or nutritional benefit? Journal of Insect Physiology, 58, 397–401.CrossRefPubMedGoogle Scholar
  21. 21.
    Put, K., Bollens, T., Wäckers, F. L., & Pekas, A. (2012). Type and spatial distribution of food supplements impact population development and dispersal of the omnivore predator Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae). Biological Control, 63, 172–180.CrossRefGoogle Scholar
  22. 22.
    Schoen, L., Ridday, G., & Lenfant, C. (2000). Side effects of different insecticides on egg hatching of the predator bug Macrolophus caliginosus (Wagner). Integrated control in Viticulture. IOBC/WPRS Bulletin, 22, 99–101.Google Scholar
  23. 23.
    Urbaneja, A., Montón, H., & Mollá, O. (2008). Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. Journal of Applied Entomology, 133, 292–296.CrossRefGoogle Scholar
  24. 24.
    van Lenteren, J. (2012). The state of commercial augmentative biological control: Plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57, 1–20.CrossRefGoogle Scholar
  25. 25.
    Wade, M. R., Zalucki, M. P., Wratten, S. D., & Robinson, K. A. (2008). Conservation biological control of arthropods using artificial food sprays: Current status and future challenges. Biological Control, 45, 185–199.CrossRefGoogle Scholar

Copyright information

© Deutsche Phythomedizinische Gesellschaft 2017

Authors and Affiliations

  • Rob Moerkens
    • 1
    • 2
    Email author
  • Els Berckmoes
    • 3
  • Veerle Van Damme
    • 4
    • 5
  • Lieve Wittemans
    • 3
  • Luc Tirry
    • 5
  • Hans Casteels
    • 4
  • Patrick De Clercq
    • 5
  • Raf De Vis
    • 3
  1. 1.Tomato ResearchProefcentrum HoogstratenHoogstratenBelgium
  2. 2.Evolutionary Ecology GroupUniversity of AntwerpAntwerpBelgium
  3. 3.Proefstation voor de GroenteteeltSint-Katelijne-WaverBelgium
  4. 4.Crop Protection, Plant Sciences UnitInstitute for Agricultural and Fisheries ResearchMerelbekeBelgium
  5. 5.Department of Crop Protection, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

Personalised recommendations