Skip to main content
SpringerLink
Log in

Impact of net houses on the natural regulation of the populations of Trialeurodes vaporariorum (Homoptera: Aleyrodidae) and Tuta absoluta (Lepidoptera: Gelechiidae), two major tomato pests in Kenya

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

The abandonment of insecticide treatments to achieve sustainable crop production calls for a combination of methods to obtain satisfactory pest control. To this end, net houses and biological control are two promising methods, though we suspected that most natural enemies are blocked outside the net houses. In Kenya, tomato crops are particularly threatened by Trialeurodes vaporariorum (Westwood 1856) and Tuta absoluta (Meyrick, 1917) that are targets of most insecticide treatments in this country. We investigated in an on-farm experiment (i) the abundances of T. vaporariorum and T. absoluta in open fields and in net houses, (ii) the diversity of arthropod natural enemies of these pests, and (iii) the effect of net houses on the natural regulation. To complete, in the laboratory, we checked the capacity of natural enemies to pass through different net types. We identified several natural enemies, mainly the mirid bug Nesidiocoris tenuis (Reuter 1895) that was the most abundant predator for both pests. One parasitoid species was also identified for each pest, i.e. Encarsia formosa Gahan (1924) and Copidosoma sp. for T. vaporariorum and T. absoluta respectively. Net houses reduced drastically the pest populations. Predators were less abundant under net houses, while parasitoids did not seem to be affected by the nets. Encarsia formosa was shown to be able to pass through the different net types, while N. tenuis adults were not. These results raise the potential for augmentative biological control under net houses. Using kairomones to attract natural enemies, or introducing natural enemies under the net houses through inoculative releases, are two approaches to increase the abundance of natural enemies under net houses.

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

Access this article

Log in via an institution

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbes K, Biondi A, Zappalà L, Chermiti B (2014) Fortuitous parasitoids of the invasive tomato leafminer Tuta absoluta in Tunisia. Phytoparasitica 42(1):85–92

    Article  Google Scholar 

  • Abbes K, Biondi A, Kurtulus A, Ricupero M, Russo A, Siscaro G, Chermiti B, Zappala L (2015) Combined non-target effects of insecticide and high temperature on the parasitoid Bracon nigricans. PLoS One 10(9):e0138411

    Article  PubMed  PubMed Central  Google Scholar 

  • Achieng’a FC, Kasina M, Mbugi J, Wasilwa L, Kariuki F, Kipyab P, Martin T (2016) Low cost insect proof and micro-climate regulating Agronets are effective in managing infestation of American Bollworm (Helicoverpa armigera Hubner.) on field tomatoes in Nairobi and Kiambu counties, Kenya. In 2nd biennial international conference on enhancing sustainable agricultural production and marketing systems (p 340)

  • 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(4):513–520

    Article  Google Scholar 

  • Ayelo PM, Pirk CWW, Yusuf AA, Chailleux A, Mohamed SA, Deletre E (2021) Exploring the kairomone-based foraging behaviour of natural enemies to enhance biological control: a review. Front Ecol Evol 9:143

    Article  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(7):803–812

    Article  CAS  PubMed  Google Scholar 

  • Blanchard EE (1940) Apuntes sobre Encirtidos Argentinos. An Soc Cient Argent 130(3):106–128

  • Bográn CE, Heinz KM, Ciomperlik MA (2002) Interspecific competition among insect parasitoids: field experiments with whiteflies as hosts in cotton. Ecology 83(3):653–668

    Article  Google Scholar 

  • Boualem M, Allaoui H, Hamadi R, Medjahed M (2012) Biologie et complexe des ennemis naturels de Tuta absoluta à Mostaganem (Algérie). EPPO Bull 42:268–274

    Article  Google Scholar 

  • CABI (2019a) Nesidiocoris tenuis (tomato bug). https://www.cabi.org/isc/datasheet/16251. Accessed 24 Jan 2020

  • CABI (2019b) Copidosoma. https://www.cabi.org/isc/datasheet/15708. Accessed 24 Jan 2020

  • 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(2):111–119

    Article  Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Khanh HDT, Maignet P, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS One 7(10)

  • Chailleux A, Desneux N, Arnó J, Gabarra R (2014) Biology of two key Palaearctic larval ectoparasitoids when parasitizing the invasive pest Tuta absoluta. J Pest Sci 87(3):441–448

    Article  Google Scholar 

  • De Bon H, Huat J, Parrot L, Sinzogan A, Martin T, Malezieux E, Vayssieres JF (2014) Pesticide risks from fruit and vegetable pest management by small farmers in sub-Saharan Africa. A review. Agron Sustain Dev 34(4):723–736

    Article  Google Scholar 

  • De Puysseleyr V, De Man S, Höfte M, De Clercq P (2013) Plantless rearing of the zoophytophagous bug Nesidiocoris tenuis. Biocontrol 58(2):205–213

    Article  Google Scholar 

  • Deletre E, Mallent M, Menut C, Chandre F, Martin T (2015) Behavioral response of Bemisia tabaci (Hemiptera: Aleyrodidae) to 20 plant extracts. J Econ Entomol 108(4):1890–1901

    Article  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KA, Burgio G, Arpaia S, Narváez-Vasquez CA, Pizzol J (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83(3):197–215

    Article  Google Scholar 

  • Diatte M, Brévault T, Sylla S, Tendeng E, Sall-Sy D, Diarra K (2018) Arthropod pest complex and associated damage in field-grown tomato in Senegal. Int J Trop Insect Sci 38(3):243–253

    Article  Google Scholar 

  • El Arnaouty SA, Kortam MN (2012) First record of the mired predatory species, Nesidiocoris tenuis Reuter (Heteroptera: Miridae) on the tomato leafminer, Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae) in Egypt. Egypt J Biol Pest Control 22(2):223

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Marine Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Gahan AB (1924) Some new parasitic Hymenoptera with notes on several described forms. Proc US Nat Mus 2517(65, Art. 4):1–23

  • Gamarra H, Carhuapoma P, Mujica M, Kreuze J, Kroschel J (2016) Greenhouse whitefly, Trialeurodes vaporariorum (Westwood 1956), in Pest distribution and risk atlas for Africa: Potential, global and regional distribution and abundance of agricultural and horticultural pests and associated biocontrol agents under current and future climates, ed. by Kroschel J, Mujica N, Carhuapoma P and Sporleder M. International Potato Center (CIP), Lima, pp 154–168

  • Gogo EO, Saidi M, Itulya FM, Martin T, Ngouajio M (2014) Eco-friendly nets and floating row covers reduce pest infestation and improve tomato (Solanum lycopersicum L.) yields for smallholder farmers in Kenya. Agronomy 4(1):1–12

    Article  Google Scholar 

  • Guillemaud T, Blin A, Le Goff I, Desneux N, Reyes M, Tabone E, Lombaert E (2015) The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci Rep 5(1):1–5

    Article  Google Scholar 

  • Guerrieri E, Noyes J (2005) Revision of the European species of Copidosoma Ratzeburg (Hymenoptera: Encyrtidae), parasitoids of caterpillars (Lepidoptera). Syst Entomol 30(1):97–174

    Article  Google Scholar 

  • Gurr GM, Kvedaras OL (2010) Synergizing biological control: scope for sterile insect technique, induced plant defences and cultural techniques to enhance natural enemy impact. Biol Control 52(3):198–207

    Article  Google Scholar 

  • Han P, Bayram Y, Shaltiel-Harpaz L, Sohrabi F, Saji A, Esenali UT, Lu ZZ (2019) Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J Pest Sci 92(4):1317–1327

    Article  Google Scholar 

  • Haran J, Delvare G, Vayssieres JF, Benoit L, Cruaud P, Rasplus JY, Cruaud A (2018) Increasing the utility of barcode databases through high-throughput sequencing of amplicons from dried museum specimens, an example on parasitic hymenoptera (Braconidae). Biol Control 122:93–100

    Article  CAS  Google Scholar 

  • Hassanpour M, Bagheri M, Golizadeh A, Farrokhi S (2016) Functional response of Nesidiocoris tenuis (Hemiptera: Miridae) to Trialeurodes vaporariorum (Hemiptera: Aleyrodidae): effect of different host plants. Biocontrol Sci Technol 26(11):1489–1503

    Article  Google Scholar 

  • Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109(3):195–219

    Article  Google Scholar 

  • Kimathi RH, Wilisiani F, Mashiko T, Neriya Y, Miinda AE, Nishigawa H, Natsuaki T (2020) First report of tomato chlorosis virus infecting tomato in Kenya. Sci Afr 7:e00286

    Google Scholar 

  • Kinyanjui G, Khamis FM, Ombura FLO, Kenya EU, Ekesi S, Mohamed SA (2021) Distribution, abundance and natural enemies of the invasive tomato leafminer, Tuta absoluta (Meyrick) in Kenya. Bull Entomol Res 1–16

  • Kungu M, Deletre E, Subramanian S, Fiaboe KK, Gitonga L, Lagat ZO, Martin T (2019) A new mite IPM strategy: predator avoidance behaviour resulting from the synergetic effects of predator release and acaricide-treated nets. Pest Manag Sci 75(4):979–985

    Article  CAS  PubMed  Google Scholar 

  • Majumdar AZ, Chambliss A, Mastin W, Carpenter S (2015) High tunnel pest exclusion system: Laboratory and field experiences. J NACAA 8(1)

  • Mansour R, Brévault T, Chailleux A, Cherif A, Grissa-Lebdi K, Haddi K, Tonnang HE (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38(2):83–112

    Article  Google Scholar 

  • Meyrick E (1917) Descriptions of South American micro-lepidoptera. Trans Entomol Soc Lond 65:1–52

    Article  Google Scholar 

  • Mound LA, SH Halsey (1978) Whiteflies of the World: A systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. British Museum (N.H.) and Wiley, Chichester, UK

  • Nannini M, Manca L, Giorgini M (2006) Natural parasitism of Bemisia tabaci and Trialeurodes vaporariorum in an horticultural area of Sardinia, Italy. IOBC WPRS Bull 29(4):59

    Google Scholar 

  • Nderitu PW, Muturi J, Otieno M, Arunga EE, Mattias J (2018) Tomato leaf miner (Tuta absoluta)(Meyrick 1917)(Lepidoptera: Gelechiidae) prevalence and farmer management practices in Kirinyanga County, Kenya. J Entomol Nematol 10(6):43–49

    Article  Google Scholar 

  • Nell HW, Lelie LSVD, Woets J, Lenteren JV (1976) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) II. Selection of host stages for oviposition and feeding by the parasite 1. Z Angew Entomol 81(1–4):372–376

    Google Scholar 

  • Njuguna NT (2000) Assessment of the level of resistance to Bifenthrin, Cypermethrin and Methomyl insecticides in Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood) whitefly populations from selected sites in Kenya (Doctoral dissertation, Kenyatta University)

  • Nordey T, Basset-Mens C, De Bon H, Martin T, Déletré E, Simon S, Parrot L, Despretz H, Huat J, Biard Y, Dubois T, Malézieux E (2017) Protected cultivation of vegetable crops in sub-Saharan Africa: limits and prospects for smallholders. A review. Agron Sustain Dev 37(6):1–20

  • Oreste M, Bubici G, Poliseno M, Tarasco E (2016) Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorum-Encarsia formosa system. J Pest Sci 89(1):153–160

    Article  Google Scholar 

  • Perić P, Dimic N (1997) Natural enemies of Trialeurodes vaporariorum Westwood in Yugoslavia. Plant Prot 48(1):67–71

    Google Scholar 

  • Perić P, Marčić D, Stamenković S (2008) Natural enemies of whitefly (Trialeurodes vaporariorum Westwood) in Serbia. In IV Balkan Symposium on Vegetables and Potatoes 830 (pp 539–544)

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 24 Jan 2020

  • Ramasamy S, Ravishankar M (2018) Integrated pest management strategies for tomato under protected structures. In Sustainable management of arthropod pests of tomato. Academic Press, pp 313–322

  • Reuter OM (1895) Ad cognitionem Capsidarum. III. Capsidae ex Africa boreali. Revue d’Entomologie, Caen 14:131–142

  • Reuter OM (1905) Ad cognitionem Capsidarum Aethiopicarum. III. Öfversigt af Finska Vetenskapssocietetens Förhandlingar 47(21):9 

  • Romeis J, Zebitz CPW (1997) Searching behaviour of Encarsia formosa as mediated by colour and honeydew. Entomol Exp Appl 82(3):299–309

    Article  Google Scholar 

  • Rwomushana I, Beale T, Chipabika G, Day R, Gonzalez-Moreno P, Lamontagne-Godwin J, Tambo J (2019) Tomato leafminer (Tuta absoluta): Impacts and coping strategies for Africa, 58p. CAB International, Wallingford

    Google Scholar 

  • Salas Gervassio NG, Luna MG, Lee S, Salvo A, Sánchez NE (2016) Trophic web associated with the South American tomato moth Tuta absoluta: implications for its conservation biological control in Argentina. Agric for Entomol 18(2):137–144

    Article  Google Scholar 

  • Scopes NEA (1969) The economics of mass rearing Encarsia formosa, a parasite of the whitefly Trialeurodes vaporariorum, for use in commercial horticulture. Plant Pathol 18(3):130–132

    Article  Google Scholar 

  • Simon S, Komlan FA, Adjaïto L, Mensah A, Coffi HK, Ngouajio M, Martin T (2014) Efficacy of insect nets for cabbage production and pest management depending on the net removal frequency and microclimate. Int J Pest Manag 60(3):208–216

    Article  Google Scholar 

  • Songa W (2003) Kenyan regulations for importation of biological control agents. Registration for biocontrol agents in Kenya 75

  • Speyer ER (1927) An important parasite of the greenhouse whitefly. Bull Entomol Res 17:301–308

    Article  Google Scholar 

  • Sridhar V, Jayashankar M, Vinesh LS (2012) Population dynamics of Zoophytophagous mirid bug, Nesidiocoris tenuis (Reuter)(Heteroptera: Miridae) and its prey, Bemisia tabaci Genn. (Homoptera: Aleyrodidae) on tomato (Solanum lycopersicum Mill). Pest Manag Hortic Ecosyst 18(1):35–38

    Google Scholar 

  • Sylla S, Brévault T, Streito JC, Diarra K (2016) First record of Nesidiocoris tenuis (Reuter)(Heteroptera: Miridae), as a predator of the tomato leaf miner, Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae). Senegal Egypt J Biol Pest Control 26(4):851–853

    Google Scholar 

  • Thomine E, Jeavons E, Rusch A, Bearez P, Desneux N (2020) 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 

  • Urbaneja A, Montón H, Molla O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133(4):292–296

    Article  Google Scholar 

  • van Lenteren JC, van Roermund HJ, Sütterlin S (1996) Biological control of greenhouse whitefly (Trialeurodes vaporariorum) with the parasitoid Encarsia formosa: How does it work? Biol Control 6(1):1–10

    Article  Google Scholar 

  • van Lenteren JC, Woets J (1988) Biological and integrated pest control in greenhouses. Annu Rev Entomol 33:239–269

    Article  Google Scholar 

  • Walker F (1838) L.—Descriptions of British Chalcidites. J Nat Hist 1(6):449–454

  • Walker F (1839) Monographia chalciditum. H. Baillière 1:333

  • Westwood JO (1856) A. vaporariorum. Gardener's Chron 852

  • Yarahmadi F, Salehi Z, Lotfalizadeh H (2018) Compatibility of insecticides and Elachertus inunctus Nees (Hymenoptera: Eulophidae) for controlling Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in greenhouse condition. J Plant Dis Prot 125(4):357–364

    Article  Google Scholar 

  • Zappala L, Biondi A, Alma A, Al-Jboory IJ, Arno J, Bayram 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

    Article  Google Scholar 

Download references

Acknowledgements

We thank the farmers for their collaboration and enriching exchanges, and Bruno Michel and Gerard Delvare for assistance with the morphological identifications. We are grateful for the financial support provided by the French National Research Agency (ANR) through CIRAD under Award No. ANR-16-CE32-0010-01.

Author information

Authors and Affiliations

  1. CIRAD, UPR HortSys, 34398, Montpellier, France

    Anaïs Chailleux & Emilie Deletre

  2. University of Montpellier, Montpellier, France

    Anaïs Chailleux, Julien M. Haran, Laure Benoit & Emilie Deletre

  3. Biopass, CIRAD-IRD-ISRA-UCAD, Dakar, Senegal

    Anaïs Chailleux

  4. International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, Kenya

    Junitor Chepkemoi, Robert Copeland & Emilie Deletre

  5. CBGP, CIRAD, Montpellier SupAgro, INRA, IRD, Univ. Montpellier, Montpellier, France

    Julien M. Haran & Laure Benoit

Authors
  1. Anaïs Chailleux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junitor Chepkemoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julien M. Haran
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laure Benoit
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert Copeland
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Emilie Deletre
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anaïs Chailleux.

Ethics declarations

Conflict of interest statement

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chailleux, A., Chepkemoi, J., Haran, J.M. et al. Impact of net houses on the natural regulation of the populations of Trialeurodes vaporariorum (Homoptera: Aleyrodidae) and Tuta absoluta (Lepidoptera: Gelechiidae), two major tomato pests in Kenya. Int J Trop Insect Sci 42, 1893–1902 (2022). https://doi.org/10.1007/s42690-021-00719-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-021-00719-w

Keywords

Search

Navigation