Simplified modelling enhances biocontrol decision making in tomato greenhouses for three important pest species

Abstract

Generalist and specialist predators are successfully used in biocontrol programs in greenhouse vegetable crops, like tomato. A greenhouse ecosystem is rather simple and provides an excellent opportunity for developing predator–prey decision models. Three systems were selected: (1) the generalist predatory bug Macrolophus pygmaeus and the greenhouse whitefly Trialeurodes vaporariorum, (2) the generalist predatory bug Nesidiocoris tenuis and the tobacco whitefly Bemisia tabaci and (3) the specialist predatory mite Phytoseiulus persimilis and the spider mite Tetranychus urticae. The study is based on an extensive field dataset. No complex mathematical predator–prey models were developed. A binomial variable was given the value of “0” for the period when the pest was not under control. As soon as the population declined after the peak density, this variable was given a value of “1”. The relationship between the densities of the prey and the predator was checked using a logistic regression model. The validated models do not calculate future pest densities but rather predict when pest control should be initiated, based on the number of pests and predators present at a certain time. Numerical simulation of the prey isoclines showed an L-shaped curve for the generalist predators and a linear curve for the specialist predators. Our simple, empirical modelling approach provides satisfactory models for biocontrol purposes. When combined with a standardized monitoring protocol, these models can be implemented in decision tools. In the future, more data will allow a machine learning approach, in which additional parameters like temperature, humidity, and time can be included.

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References

  1. Alatawi F, Nechols JR, Margolies DC (2011) Spatial distribution of predators and prey affect biological control of twospotted spider mites by Phytoseiulus persimilis in greenhouses. Biol Control 56:36–42. https://doi.org/10.1016/j.biocontrol.2010.09.006

    Article  Google Scholar 

  2. Alomar O, Riudavets J, Castañé C (2006) Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biol Control 36:154–162. https://doi.org/10.1016/j.biocontrol.2005.08.010

    Article  Google Scholar 

  3. Bancroft JS, Margolies DC (1999) An individual-based model of an acarine tritrophic system: lima bean, Phaseolus lunatus L., twospotted spider mite, Tetranychus urticae (Acari: Tetranychidae), and Phytoseiulus persimilis (Acari: Phytoseiidae). Ecol Model 123:161–181. https://doi.org/10.1016/S0304-3800(99)00131-3

    Article  Google Scholar 

  4. Bernstein C (1985) A simulation model for an acarine predator-prey system (Phytoseiulus persimilis-Tetranychus urticae). J Anim Ecol 54:375–389. https://doi.org/10.2307/4485

    Article  Google Scholar 

  5. 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). J Pest Sci 77:211–219. https://doi.org/10.1007/s10340-004-0057-2

    Article  Google Scholar 

  6. Böckmann E, Hommes M, Meyhöfer R (2015) Yellow traps reloaded: what is the benefit for decision making in practice? J Pest Sci 88:439–449. https://doi.org/10.1007/s10340-014-0601-7

    Article  Google Scholar 

  7. Brenard N, Sluydts V, De Bruyn L, Leirs H, Moerkens R (2018) Food supplementation to optimize inoculative release of the predatory bug Macrolophus pygmaeus in sweet pepper. Entomol Exp Appl 166:574–582. https://doi.org/10.1111/eea.12704

    CAS  Article  Google Scholar 

  8. Brenard N, Sluydts V, Christianen E, Bosmans L, De Bruyn L, Moerkens R, Leirs H (2019) Biweekly supplementation with Artemia spp cysts allows efficient population establishment by Macrolophus pygmaeus in sweet pepper. Entomol Exp Appl. https://doi.org/10.1111/eea.12776

    Article  Google Scholar 

  9. 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. https://doi.org/10.1007/s10526-012-9455-1

    Article  Google Scholar 

  10. Calvo FJ, Lorente MJ, Stansly PA, Belda JE (2012b) Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisia tabaci in greenhouse tomato. Entomol Exp Appl 143:111–119. https://doi.org/10.1111/j.1570-7458.2012.01238.x

    Article  Google Scholar 

  11. Carnero A, Diaz S, Amador S, Hernandez M, Hernandez E (2000) Impact of Nesidiocoris tenuis (Heteroptera, Miridae) on whitefly populations in protected tomato crops. Bulletin IOBC/wprs 23:259

    Google Scholar 

  12. Castañé C, Aloma O, Goula M, Gabarra R (2004) Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biol Control 30:591–597. https://doi.org/10.1016/j.biocontrol.2004.02.012

    Article  Google Scholar 

  13. Drukker B, Janssen A, Ravensberg W, Sabelis MW (1997) Improved control capacity of the mite predator Phytoseiulus persimilis (Acari: Phytoseiidae) on tomato. Expl Appl Acarol 21:507–518. https://doi.org/10.1023/B:APPA.0000018885.35044.c6

    Article  Google Scholar 

  14. Enkegaard A, Brodsgaard 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. https://doi.org/10.1023/A:1019230603364

    Article  Google Scholar 

  15. Frans M, Moerkens R, Van Gool S, Sauviller C, Van Laethem S, Luca S, Aerts R, Ceusters J (2018) Modelling greenhouse climate factors to constrain internal fruit rot (Fusarium spp.) in bell pepper. J Plant Dis Prot 125:425–432. https://doi.org/10.1007/s41348-018-0159-3

    Article  Google Scholar 

  16. Gause GF, Smaragdova NP, Witt AA (1936) Further studies of interaction between predators and prey. J Anim Ecol 5:1–18. https://doi.org/10.2307/1087

    Article  Google Scholar 

  17. Gough N (1991) Long-term stability in the interaction between Tetranychus urticae and Phytoseiulus persimilis producing successful integrated control on roses in southeast Queensland. Exp Appl Acarol 12:83–101. https://doi.org/10.1007/BF01204402

    Article  Google Scholar 

  18. Hanski I, Hansson L, Henttonen H (1991) Specialist predators, generalist predators, and the microtine rodent cycle. J Anim Ecol 60:353–367. https://doi.org/10.2307/5465

    Article  Google Scholar 

  19. Hanski I, Hentonnen H, Korpimäki E, Oksanen L, Turchin P (2001) Small-rodent dynamics and predation. Ecology 82:1505–1520. https://doi.org/10.2307/2679796

    Article  Google Scholar 

  20. Ingegno BI, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181. https://doi.org/10.1016/j.biocontrol.2011.06.003

    Article  Google Scholar 

  21. Kozlova I, Singh M, Easton A, Ridland P (2005) Twospotted spider mite predator-prey model. Math Comput Model 42:1287–1298. https://doi.org/10.1016/j.mcm.2005.01.036

    Article  Google Scholar 

  22. Křivan V (1996) Optimal Foraging and Predator-Prey Dynamics. Theor Pop Biol. 49:265–290. https://doi.org/10.1006/tpbi.1996.0014

    Article  Google Scholar 

  23. Křivan V (2011) On the Gause predator-prey model with a refuge: a fresh look at the history. J Theor Biol 274:67–73. https://doi.org/10.1016/j.jtbi.2011.01.016

    Article  PubMed  Google Scholar 

  24. Křivan V, Priyadarshi A (2015) L-shaped prey isocline in the Gause predator-prey experiments with a prey refuge. J Theor Biol 370:21–26. https://doi.org/10.1016/j.jtbi.2015.01.021

    Article  PubMed  Google Scholar 

  25. Kuang Y, Ben-Arieh B, Zhao S, Wu CH, Margolies D, Nechols J (2017) Mathematical model for two-spotted spider mites system: verification and validation. Open J Model Simul 5:13–31. https://doi.org/10.4236/ojmsi.2017.51002

    Article  Google Scholar 

  26. Messelink G, Janssen A (2014) Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation. Biol Control 79:1–7. https://doi.org/10.1016/j.biocontrol.2014.07.009

    Article  Google Scholar 

  27. Moerkens R, Berckmoes E, Van Damme V, Ortega-Parra N, Hanssen I, Wutack M, Wittemans L, Casteels H, Tirry L, De Clercq P, De Vis R (2016a) High population densities of Macrolophus pygmaeus on tomato plants can cause economic fruit damage: interaction with Pepino mosaic virus? Pest Manag Sci 72:1350–1358. https://doi.org/10.1002/ps.4159

    CAS  Article  PubMed  Google Scholar 

  28. Moerkens R, Vanlommel W, Vanderbruggen R, Van Delm T (2016b) The added value of LED assimilation light in combination with high pressure sodium lamps in protected tomato crops in Belgium. Acta Hortic 1134:119–124. https://doi.org/10.17660/ActaHortic.2016.1134.16

    Article  Google Scholar 

  29. Moerkens R, Berckmoes E, Van Damme V, Wittemans L, Tirry L, Casteels H, De Clercq P, De Vis R (2017) Inoculative release strategies of Macrolophus pygmaeus Rambur (Hemiptera: Miridae) in tomato crops: population dynamics and dispersal. J Plant Dis Prot 124:295–303. https://doi.org/10.1007/s41348-017-0077-9

    Article  Google Scholar 

  30. Moerkens R, Brenard N, Bosmans L, Reybroeck E, Janssen D, Hemming J, Sluydts V (2019) Protocol for semi-automatic identification of whiteflies Bemisia tabaci and Trialeurodes vaporariorum on yellow sticky traps. J Appl Entomol. https://doi.org/10.1111/jen.12630

    Article  Google Scholar 

  31. Mukhopadhyay B, Bhattacharyya R (2013) Vole population dynamics under the influence of specialist and generalist predation. Nat Resour Model 26:91–110. https://doi.org/10.1111/j.1939-7445.2012.00122.x

    Article  Google Scholar 

  32. Nomikou M, Janssen A, Schraag R, Sabelis MW (2002) Phytoseiid predators suppress populations of Bemisia tabaci on cucumber plants with alternative food. Exp Appl Acarol 27:57–68. https://doi.org/10.1023/A:1021559421344

    Article  PubMed  Google Scholar 

  33. Opit GP, Nechols JR, Margolies DC (2004) Biological control of twospotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), using Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on ivy geranium: assessment of predator release ratios. Biol Control 29:445–452. https://doi.org/10.1016/j.biocontrol.2003.08.007

    Article  Google Scholar 

  34. Perdikis D, Lykouressis D (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biol Control 17:55–60. https://doi.org/10.1006/bcon.1999.0774

    Article  Google Scholar 

  35. Perdikis D, Lykouressis D (2002) Life table and biological characteristics of Macrolophus pygmaeus when feeding on Myzus persicae and Trialeurodes vaporariorum. Entomol Exp Appl 102:261–272. https://doi.org/10.1046/j.1570-7458.2002.00947.x

    Article  Google Scholar 

  36. Pinto-Zevallos Vänninen I (2013) Yellow sticky traps for decision-making in whitefly management: What has been achieved? Crop Protection 47:74–84. https://doi.org/10.1016/j.cropro.2013.01.009

    Article  Google Scholar 

  37. Rosenzweig ML, MacArthur RH (1963) Graphical representation and stability conditions of predator–prey interactions. Am Nat 97:209–223. https://doi.org/10.1086/282272

    Article  Google Scholar 

  38. Symondson WOC, Sunderland KD, Greenstone HM (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594. https://doi.org/10.1146/annurev.ento.47.091201.145240

    CAS  Article  PubMed  Google Scholar 

  39. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  40. Turchin P, Hanski I (1997) An empirically based model for latitudinal gradient in vole population dynamics. Am Nat 149:842–874. https://doi.org/10.1086/286027

    CAS  Article  PubMed  Google Scholar 

  41. Urbaneja A, Montón H, Mollá O (2009) Suitability of the tomato borer Tuta absoluta as prey or Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133:292–296. https://doi.org/10.1111/j.1439-0418.2008.01319.x

    Article  Google Scholar 

  42. 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. https://doi.org/10.1002/ps.3344

    CAS  Article  PubMed  Google Scholar 

  43. Urbaneja-Bernat P, Bru P, González-Cabrera J, Urbaneja A, Tena A (2019) Reduced phytophagy in sugar-provisioned mirids. J Pest Sci. https://doi.org/10.1007/s10340-019-01105-9

    Article  Google Scholar 

  44. van Baalen M, Krivan V, van Rijn PCJ, Sabelis M (2001) Alternative food, switching predators, and the persistence of predator-prey systems. Am Naturalist 157:512–524. https://doi.org/10.1086/319933

    Article  Google Scholar 

  45. Van Lenteren JC, Van Roermund HJW, Sütterlin S (1996) Biological Control of Greenhouse Whitefly (Trialeurodes vaporariorum) with the Parasitoid Encarsia formosa: How Does It Work? Biol Control 6:1–10. https://doi.org/10.1006/bcon.1996.0001

    Article  Google Scholar 

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Acknowledgements

The Agency Flanders Innovation & Entrepreneurship (VLAIO) financed this study. The research Project 140948 was granted to Research Centre Hoogstraten (R. Moerkens, L. Bosmans) in cooperation with Research Station for Vegetable Production (E. Reybroeck) and the University of Antwerp (V. Sluydts, H. Leirs). A second VLAIO project (160427) expanded the previous consortium with the Andalusian Institute for Research and Training in Agriculture and Fishery (APCIN2016-00034-00-00) (D. Janssen) and Wageningen University and Research. There is no conflict of interest.

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The Agency Flanders Innovation & Entrepreneurship (VLAIO) (140948, 160427)

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Moerkens, R., Janssen, D., Brenard, N. et al. Simplified modelling enhances biocontrol decision making in tomato greenhouses for three important pest species. J Pest Sci 94, 285–295 (2021). https://doi.org/10.1007/s10340-020-01256-0

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Keywords

  • Bemisia tabaci
  • Biocontrol
  • Macrolophus pygmaeus
  • Nesidiocoris tenuis
  • Phytoseiulus persimilis
  • Tetranychus urticae
  • Trialeurodes vaporariorum