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Field application of entomopathogenic nematodes against Thaumatotibia leucotreta in South African avocado, litchi and macadamia orchards

  • Willem P. SteynEmail author
  • Mieke S. Daneel
  • Antoinette P. Malan


False codling moth, Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae), is an important pest of fruit trees in South Africa. The subtropical fruit tree crop industries use a combination of techniques for T. leucotreta suppression. Semi-field trials were conducted in avocado, litchi and macadamia orchards, using four entomopathogenic nematode (EPN) species. The effect on T. leucotreta mortality, directly after application (two days), as well as on persistence for 7, 14, 21, 28, 35, and 42 days post-application, was determined. Results from the field trials, using 30 IJs cm2 of Steinernema yirgalemense, showed the highest mortality of 86% directly after application, with Steinernema litchii being the least effective of the four EPN species, with 63% mortality. High persistence was found until day 14, with a steep decline thereafter until day 28. Local South African EPN species showed great potential for the future control of the late instar T. leucotreta, with the added advantage of persistence.


False codling moth Heterorhabditis Persistence Semi-field trials Steinernema 



The authors wish to thank the South African Avocado Growers’ Association (SAAGA) and the South African Macadamia Growers’ Association (SAMAC) for financial assistance during the present study, in terms of project P03000039 of the ARC-TSC. Additional thanks are due to the National Research Foundation (THRIP-TP14062571871), as well as to River Bioscience, for supplying the false codling moth larvae used during the field trials. The technical assistance of Charles Arries, Thuli Selabela, Rachel Mohlala, and Dr Akhona Mbatyoti from the ARC-TSC is also appreciated.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abate AA, Slippers B, Wingfield MJ, Malan AP, Hurley BP (2018) Diversity of entomopathogenic nematodes and their symbiotic bacteria in South African plantations and indigenous forests. Nematology 20:355–371CrossRefGoogle Scholar
  2. Abd-Elgawad MMM, Askary TH, Coupland J (2017) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CABI, WallingfordCrossRefGoogle Scholar
  3. Addis T, Mijušković N, Strauch O, Ehlers R-U (2016) Life history traits, liquid culture production and storage temperatures of Steinernema yirgalemense. Nematology 18:367–376CrossRefGoogle Scholar
  4. Boemare N, Givaudan A, Brehelin M, Laumond C (1997) Symbiosis and pathogenicity of nematode-bacterium complexes. Symbiosis 22:21–45Google Scholar
  5. CABI (Centre for Agriculture and Bioscience International) (2011) Crop protection compendium. Thaumatotibia leucotreta. CABI, Wallingford.
  6. Campos-Herrera R (2015) Nematode pathogenesis of insects and other pests: ecology and applied technologies for sustainable plant and crop protection. Springer, BaselCrossRefGoogle Scholar
  7. De Waal JY, Malan AP, Addison MF (2011) Efficacy of entomopathogenic nematodes (Rhabditida: Heterorhabditidae and Steinernematidae) against codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in temperate regions. Biocontrol Sci Technol 20:489–502CrossRefGoogle Scholar
  8. Duncan LW, Graham JH, Dunn JC, Zellers J, McCoy CW, Nguyen K (2003) Incidence of endemic entomopathogenic nematodes following application of Steinernema riobrave for control of Diaprepes abbreviatus. J Nematol 5:178–186Google Scholar
  9. Forst S, Clarke D (2002) Bacteria-nematode symbiosis. In: Gaugler R (ed) Entomopathogenic nematology. CABI, Wallingford, pp 55–77Google Scholar
  10. Georgis R, Kaya HK, Gaugler R (1991) Effect of steinernematid and heterorhabditid nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) on nontarget arthropods. Environ Entomol 20:815–822CrossRefGoogle Scholar
  11. Glazer I, Lewis EE (2000) Bioassays for entomopathogenic microbes and nematodes. In: Navon A, Ascher K (eds) Bioassays of entomopathogenic microbes and nematodes. CABI, Wallingford, pp 229–247CrossRefGoogle Scholar
  12. Griffin CT, Boemare NE, Lewis EE (2005) Biology and behaviour. In: Grewal P, Ehlers R-U, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 47–64CrossRefGoogle Scholar
  13. Hatting JL, Malan AP (2017) Status of entomopathogenic nematodes in integrated pest management strategies in South Africa. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CABI, Wallingford, pp 409–428CrossRefGoogle Scholar
  14. Hatting J, Stock SP, Hazir S (2009) Diversity and distribution of entomopathogenic nematodes (Steinernematidae, Heterorhabditidae) in South Africa. J Invertebr Pathol 102:120–128CrossRefGoogle Scholar
  15. Hatting JL, Moore SD, Malan AP (2019) Microbial control of phytophagous invertebrate pests in South Africa: current status and future. J Invertebr Pathol (in press). Google Scholar
  16. Le Vieux PD, Malan AP (2015) Prospects for using entomopathogenic nematodes to control the vine mealybug, Planococcus ficus, in South African vineyards. S Afr J Enol Vitic 36:59–70Google Scholar
  17. Malan AP, Ferreira T (2017) Entomopathogenic nematodes. In: Fourie H, Spaull VW, Jones RK, Daneel M, De Waele D (eds) Nematology in South Africa: a view from the 21st century. Springer, Basel, pp 459–480CrossRefGoogle Scholar
  18. Malan AP, Hatting J (2015) Entomopathogenic nematode exploitation: case studies in laboratory and field applications from South Africa. In: Campos-Herrera R (ed) Sustainability in plant and crop protection: ecology and applied technologies for sustainable plant and crop protection. Springer, Switzerland, pp 475–506Google Scholar
  19. Malan AP, Moore SD (2016) Evaluation of local entomopathogenic nematodes for the control of false codling moth, Thaumatotibia leucotreta (Meyrick, 1913), in a citrus orchard in South Africa. Afr Entomol 24:489–501CrossRefGoogle Scholar
  20. Malan AP, Nguyen KB, Addison MF (2006) Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) from the southwestern parts of South Africa. Afr Plant Prot 12:65–69Google Scholar
  21. Malan AP, Knoetze R, Moore SD (2011) Isolation and identification of entomopathogenic nematodes from citrus orchards in South Africa and their biocontrol potential against false codling moth. J Invertebr Pathol 108:115–125CrossRefGoogle Scholar
  22. Malan AP, Von Diest JI, Moore SM, Addison P (2018) Control options for false codling moth, Thaumatotibia leucotreta (Lepidoptera: Tortricidae), in South Africa, with emphasis on the potential use of entomopathogenic nematodes and fungi. Afr Entomol 26:14–29CrossRefGoogle Scholar
  23. Nguyen KB, Tesfamariam M, Gozel U, Gaugler R, Adams BJ (2004) Steinernema yirgalemense n. sp. (Rhabditida: Steinernematidae) from Ethiopia. Nematology 6:839–856CrossRefGoogle Scholar
  24. Nguyen KB, Malan AP, Gozel U (2006) Steinernema khoisanae n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from South Africa. Nematology 8:157–175CrossRefGoogle Scholar
  25. Odendaal D, Addison MF, Malan AP (2016a) Entomopathogenic nematodes for the control of codling moth (Cydia pomonella L.) in field and laboratory trials. J Helminthol 90:615–625CrossRefGoogle Scholar
  26. Odendaal D, Addison MF, Malan AP (2016b) Evaluation of above-ground application of entomopathogenic nematodes for control of codling moth (Cydia pomonella L.) under natural conditions. Afr Entomol 24:61–74CrossRefGoogle Scholar
  27. Poinar GO Jr (1976) Description and biology of a new insect parasitic rhabditoid, Heterorhabditis bacteriophora n. gen. n. sp. (Rhabditida; Heterorhabditidae n. fam.). Nematologica 21:463–470CrossRefGoogle Scholar
  28. Poinar GO Jr (1990) Taxonomy and biology of Steinernematidae and Heterorhabditidae. In: Gauler R, Kaya H (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 23–60Google Scholar
  29. Prinsloo GL, Uys VM (2015) Insects of cultivated plants and natural pastures in Southern Africa. Entomological Society of Southern Africa, PretoriaGoogle Scholar
  30. Shapiro-Ilan D, Gouge DH, Koppenhöfer AM (2002) Factors affecting commercial success: case studies in cotton, turf and citrus. In: Gaugler R (ed) Entomopathogenic nematology. CABI, Wallingford, pp 333–355CrossRefGoogle Scholar
  31. Shapiro-Ilan DI, Duncan LW, Lacey LA, Han R (2005) Orchard applications. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 205–229Google Scholar
  32. Snedecor GW, Cochran WG (1991) Statistical methods, 8th edn. Iowa State University Press, Iowa CityGoogle Scholar
  33. Spiridonov SE, Subbotin SA (2016) Phylogeny and phytogeography of Heterorhabditis and Steinernema. In: Hunt DJ, Nguyen KB (eds) Advances in entomopathogenic nematode taxonomy and phylogeny. Brill, Leiden, pp 413–427Google Scholar
  34. Steyn WP, Malan AP, Daneel MS, Slabbert MM (2017a) Entomopathogenic nematodes from north-eastern South Africa and their virulence against the false codling moth, Thaumatotibia leucotreta (Lepidoptera: Tortricidae). Biocontrol Sci Technol 19:1265–1278CrossRefGoogle Scholar
  35. Steyn WP, Knoetze R, Tiedt LR, Malan AP (2017b) Steinernema litchii n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from South Africa. Nematology 19:1157–1177CrossRefGoogle Scholar
  36. Stokwe NF, Malan AP (2016) Susceptibility of the obscure mealybug, Pseudococcus viburni (Signoret) (Pseudococcidae), to South African isolates of entomopathogenic nematodes. Int J Pest Manage 62:119–128CrossRefGoogle Scholar
  37. Stuart RJ, Borai EFE, Duncan LW (2008) From augmentation to conservation of entomopathogenic nematodes: trophic cascades, habitat manipulation and enhanced biological control of Diaprepes abbreviates root weevils in Florida citrus groves. J Nematol 40:73–84Google Scholar
  38. Subtrop (Subtropical Fruit Growers Association) (2016).
  39. Toepfer S, Hatala-Zselle I, Ehlers R-U, Peters A, Kuhlmann U (2010) The effect of application techniques on field-scale efficacy: can the use of entomopathogenic nematodes reduce damage by western corn rootworm larvae? Agric For Entomol 12:389–402CrossRefGoogle Scholar
  40. van Niekerk S, Malan AP (2012) Potential of South African entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) for control of the citrus mealybug, Planococcus citri (Pseudococcidae). J Invertebr Pathol 111:166–174CrossRefGoogle Scholar
  41. Wright DJ, Peters A, Schroer S, Fife JP (2005) Application technology. In: Grewal P, Ehlers R, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 91–106CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2019

Authors and Affiliations

  1. 1.Agricultural Research Council – Tropical and Subtropical CropsNelspruitSouth Africa
  2. 2.Department of Conservation, Ecology and Entomology, Faculty of AgriSciencesStellenbosch UniversityStellenboschSouth Africa

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