pp 1–9 | Cite as

Effect of supplementary food containing Artemia salina on the development and survival of flightless Harmonia axyridis in greenhouses

  • Tomokazu SekoEmail author
  • Junichiro Abe
  • Kazuki Miura


Brine shrimp cysts are potentially useful as a supplemental food to sustain populations of flightless Harmonia axyridis Pallas in greenhouses. We studied the effect of Artemia salina L., alone and combined with sucrose, on the survival and development of juvenile flightless H. axyridis under laboratory conditions. The proportion of wing malformations, the body size of females, and the hatching rate were improved by the addition of sucrose to diets containing Artemia cysts alone. We conducted release experiments in greenhouses containing eggplants to evaluate the effects of the supplemental food, consisting of a mixture of A. salina and sucrose. Compared with non-supplemented eggplants, more larvae, pupae, and adults of flightless H. axyridis were observed and the incidence of aphids tended to be suppressed in the plots with supplemental food. These results show that the food supplementation effectively improves the development and survival of juvenile flightless H. axyridis during periods of low prey density.


Brine shrimp cysts Artemia salina Supplemental food Flightless strain Harmonia axyridis Greenhouse 



We especially thank T. Oishi for technical support in the greenhouses at the NARO Western Region Agricultural Research Center. This work was supported in part by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan through the Science and Technology Research Promotion Program for agriculture, forestry, fisheries and food industries (No. 28021C). Two anonymous reviewers provided helpful comments on an earlier version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Arijs Y, De Clercq P (2001) Rearing Orius laevigatus on cysts of the brine shrimp Artemia franciscana. Biol Control 21:79–83CrossRefGoogle Scholar
  2. Bonte M, Samih MA, De Clercq P (2010) Development and reproduction of Adalia bipunctata on factitious and artificial foods. BioControl 55:485–491CrossRefGoogle Scholar
  3. Castañé C, Quero R, Riudavets J (2006) The brine shrimp Artemia sp as alternative prey for rearing the predatory bug Macrolophus caliginosus. Biol Control 38:405–412CrossRefGoogle Scholar
  4. Cohen AC, Smith LK (1998) A new concept in artificial diets for Chrysoperla rufilabris: the efficacy of solid diets. Biol Control 13:49–54CrossRefGoogle Scholar
  5. De Clercq P, Arijs Y, van Meir T, van Stappen G, Sorgeloos P, Dewettinck K, Rey M, Grenier S, Febvay G (2005) Nutritional value of brine shrimp cysts as a factitious food for Orius laevigatus (Heteroptera: Anthocoridae). Biocontrol Sci Technol 15:467–479CrossRefGoogle Scholar
  6. Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecol Entomol 25:140–146CrossRefGoogle Scholar
  7. Everitt BS, Hothorn T (2010) A handbook of statistical analyses using R, 2nd edn. CRC Press, Boca RatonGoogle Scholar
  8. Hongo T, Obayashi N (1997) Use of diapause eggs of brine shrimp, Artemia salina (Linne) for artificial diet of coccinellid beetle, Harmonia axyridis (Pallas). Jpn J Appl Ent Zool 41:101–105CrossRefGoogle Scholar
  9. Koss AM, Snyder WE (2005) Alternative prey disrupt biocontrol by a guild of generalist predators. Biol Control 32:243–251CrossRefGoogle Scholar
  10. Leman A, Messelink GJ (2015) Supplemental food that supports both predator and pest: a risk for biological control? Exp Appl Acarol 65:511–524CrossRefGoogle Scholar
  11. Lommen STE, Middendorp CW, Luijten CA, van Schelt J, Brakefield PM, de Jong PW (2008) Natural flightless morphs of the ladybird beetle Adalia bipunctata improve biological control of aphids on single plants. Biol Control 47:340–346CrossRefGoogle Scholar
  12. Lundgren JG (2009) Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae. Biol Control 51:294–305CrossRefGoogle Scholar
  13. Madsen M, Terkildsen S, Toft S (2004) Microcosm studies on control of aphids by generalist arthropod predators: effects of alternative prey. BioControl 49:483–504CrossRefGoogle Scholar
  14. 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 59:377–393CrossRefGoogle Scholar
  15. Messelink GJ, Bloemhard CMJ, Hoogerbrugge H, van Schelt J, Ingegno BL, Tavella L (2015) Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper. J Appl Entomol 139:333–341CrossRefGoogle Scholar
  16. Messelink GJ, Vijverberg R, Leman A, Janssen A (2016) Biological control of mealybugs with lacewing larvae is affected by the presence and type of supplemental prey. BioControl 61:555–565CrossRefGoogle Scholar
  17. 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 Protect 124:295–303CrossRefGoogle Scholar
  18. Nakayama S, Seko T, Takatsuki J, Miura K, Miyatake T (2010) Walking activity of flightless Harmonia axyridis (Coleoptera: Coccinellidae) as a biological control agent. J Econ Entomol 103:1564–1568CrossRefGoogle Scholar
  19. Nguyen DT, Vangansbeke D, De Clercq P (2014a) Solid artificial diets for the phytoseiid predator Amblyseius swirskii. BioControl 59:719–727CrossRefGoogle Scholar
  20. Nguyen DT, Vangansbeke D, De Clercq P (2014b) Artificial and factitious foods support the development and reproduction of the predatory mite Amblyseius swirskii. Exp Appl Acarol 62:181–194CrossRefGoogle Scholar
  21. Nguyen DT, Vangansbeke D, De Clercq P (2015) Performance of four species of phytoseiid mites on artificial and natural diets. Biol Control 80:56–62CrossRefGoogle Scholar
  22. Nishimori T, Miura K, Seko T (2016) Rearing Orius strigicollis (Hemiptera: Anthocoridae) on an alternative diet of brine shrimp, Artemia salina (Anostraca: Artemiidae). Appl Entomol Zool 51:321–325CrossRefGoogle Scholar
  23. R Development Core Team (2011) In: R: a language and environment for statistical computing. R Foundation, Vienna.
  24. Riddick EW, Wu Z, Rojas G (2014) Potential utilization of Artemia franciscana eggs as food for Coleomegilla maculata. BioControl 59:575–583CrossRefGoogle Scholar
  25. Schumacher SK, Marsh TL, Williams KA (2006) Optimal pest control in greenhouse production of ornamental crops. Agric Econ 34:39–50CrossRefGoogle Scholar
  26. Seko T (2015) Augmentative release of flightless Harmonia axyridis in greenhouses with cultivated vegetables. JATAFF J 3:9–13Google Scholar
  27. Seko T, Yamashita K, Miura K (2008) Residence period of a flightless strain of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in open fields. Biol Control 47:194–198CrossRefGoogle Scholar
  28. Seko T, Miyatake T, Miura K (2012) Assessment of hybrid vigor between flightless lines to restore survival and reproductive characteristics in the ladybird beetle Harmonia axyridis. BioControl 57:85–93CrossRefGoogle Scholar
  29. Seko T, Sumi A, Nakano A, Kameshiro M, Kaneda T, Miura K (2014) Suppression of aphids by augmentative release of larvae of flightless Harmonia axyridis. J Appl Entomol 138:326–337CrossRefGoogle Scholar
  30. Seko T, Abe J, Miura K, Hikawa M (2017) The contribution of a beneficial insectary plant Scaevola aemula to survival and long-term establishment of flightless Harmonia axyridis in greenhouses. BioControl 62:221–231CrossRefGoogle Scholar
  31. Sighinolfi L, Febvay G, Dindo ML, Rey M, Pageaux J, Baronio P, Grenier S (2008) Biological and biochemical characteristics for quality control of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) reared on a liver-based diet. Arch Insect Biochem Physiol 68:26–39CrossRefGoogle Scholar
  32. Sighinolfi L, Febvay G, Dindo ML, Rey M, Pageaux J, Grenier S (2013) Biochemical content in fatty acids and biological parameters of Harmonia axyridis reared on artificial diet. Bull Insectol 66:283–290Google Scholar
  33. Sun Y-X, Hao Y-N, Riddick EW, Liu T-X (2017) Factitious prey and artificial diets for predatory lady beetles: current situation, obstacles, and approaches for improvement: a review. Biocontrol Sci Technol 27:601–619CrossRefGoogle Scholar
  34. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594CrossRefGoogle Scholar
  35. Tourniaire R, Ferran A, Gambier J, Giuge L, Bouffault F (1999) Locomotor behavior of flightless Harmonia axyridis Pallas (Col., Coccinellidae). J Insect Behav 12:545–558CrossRefGoogle Scholar
  36. van Rijn PC, Tanigoshi LK (1999) The contribution of extrafloral nectar to survival and reproduction of the predatory mite Iphiseius degenerans on Ricinus communis. Exp Appl Acarol 23:281–296CrossRefGoogle Scholar
  37. Vandekerkhove B, Parmentier L, van Stappen G, Grenier S, Febvay G, Rey M, De Clercq P (2009) Artemia cysts as an alternative food for the predatory bug Macrolophus pygmaeus. J Appl Entomol 133:133–142CrossRefGoogle Scholar
  38. Vangansbeke D, Nguyen DT, Audenaert J, Verhoeven R, Gobin B, Tirry L, De Clercq P (2014a) Performance of the predatory mite Amblydromalus limonicus on factitious foods. BioControl 59:67–77CrossRefGoogle Scholar
  39. Vangansbeke D, Nguyen DT, Audenaert J, Verhoeven R, Gobin B, Tirry L, De Clercq P (2014b) Food supplementation affects interactions between a phytoseiid predator and its omnivorous prey. Biol Control 76:95–100CrossRefGoogle Scholar
  40. Vangansbeke D, Nguyen DT, Audenaert J, Verhoeven R, Gobin B, Tirrya L, De Clercq P (2016) Supplemental food for Amblyseius swirskii in the control of thrips: feeding friend or foe? Pest Manag Sci 72:466–473CrossRefGoogle Scholar
  41. Wade MR, Zalucki MP, Wratten SD, Robinson KA (2008) Conservation biological control of arthropods using artificial food sprays: current status and future challenges. Biol Control 45:185–199CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2019

Authors and Affiliations

  1. 1.National Agriculture and Food Research Organization Western Region Agricultural Research CenterFukuyamaJapan

Personalised recommendations