Advertisement

BioControl

, Volume 59, Issue 6, pp 729–738 | Cite as

Prey range of the predatory ladybird Cryptolaemus montrouzieri

  • Sara Maes
  • Jean-Claude Grégoire
  • Patrick De Clercq
Article

Abstract

The prey range of Cryptolaemus montrouzieri was studied in the laboratory to investigate whether the mealybug destroyer can contribute to the suppression of other pest insects besides mealybugs and to assess its potential impact on non-mealybug populations as part of an environmental risk assessment for its use in biological control. Prey tested in these experiments were: tobacco aphid Myzus persicae nicotianae (Sulzer)(Hemiptera: Aphididae), pea aphid Acyrthosiphon pisum (Harris)(Hemiptera: Aphididae), tobacco whitefly Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae), southern green stinkbug Nezara viridula (L.)(Hemiptera: Pentatomidae) eggs, western flower thrips Frankliniella occidentalis (Pergande)(Thysanoptera: Thripidae), two-spotted ladybird Adalia bipunctata (L.)(Coleoptera: Coccinellidae) eggs and eggs of the greater wax moth Galleria mellonella L. (Lepidoptera: Pyralidae). Larval survival was high to moderate when C. montrouzieri was provided with hemipteran prey and poor to zero when the ladybirds were provided with non-hemipteran prey. Females reared on M. persicae and A. pisum produced similar numbers of eggs as their counterparts fed the citrus mealybug Planococcus citri (Risso)(Hemiptera: Pseudococcidae), but fecundity was significantly lower when the ladybirds were reared on B. tabaci nymphs or on A. bipunctata eggs. Prey species that were found to be less suitable for immature development of C. montrouzieri could still be an adequate food source for reproduction and survival of adult ladybirds. For example, only 8 % of the predator larvae reached the adult stage when provided with A. bipunctata eggs, but females that had developed on eggs of the Mediterranean flour moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) and that were supplied with A. bipunctata eggs from adult emergence on, were only 35 % less fecund than females provided with mealybugs in their adult life. The results are discussed in relation to the development of a suitable methodology for prey/host range testing in the framework of an environmental risk assessment for arthropod natural enemies.

Keywords

Biological control Environmental risk assessment Prey range Non-native species Predator Coleoptera Coccinellidae 

Notes

Acknowledgments

We would like to thank three anonymous reviewers and handling editor Arne Janssen for their constructive comments. This research was supported by BOF (UGent).

References

  1. Albajes R, Alomar O (1999) Current and potential use of polyphagous predators. In: Albajes R, Lodovica Gullino M, van Lenteren JC, Elad Y (eds) Integrated pest and disease management in greenhouse crops. Kluwer Acad Publ, Dordrecht, The Netherlands, pp 265–275CrossRefGoogle Scholar
  2. Attia AR, Afifi AI, El-Arnaouty SA, Alla AEA (2011) Feeding potential of the predator, Cryptolaemus montrouzieri Mulsant on eggs, nymphs and adults of Planococcus citri and Ephestia kuehniella eggs. Egypt J Biol Pest Control 21:291–296Google Scholar
  3. Babendreier D, Bigler F, Kuhlmann U (2005) Methods used to assess non-target effects of invertebrate biological control agents of arthropod pests. BioControl 50:821–870CrossRefGoogle Scholar
  4. Bale JS (2011) Harmonisation of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions. In: Ehlers RU (ed) Regulation of biological control agents in Europe. Springer Science and Business Media B.V, The Netherlands, pp 323–374CrossRefGoogle Scholar
  5. Berkvens N, Baverstock J, De Clercq P, Majerus MEN, Pell JK, Roy HE, Tirry L, Wells P (2009) Good and bad traits of Harmonia axyridis-From biological control to invasion. In: Mason PG, Gillespie DR, Vincent C (eds) Proceedings of 3rd international symposium on biological control for arthropods, pp 394–402Google Scholar
  6. Bourgoin T, Campbell BC (2002) Inferring a phylogeny for hemiptera: falling into the ‘Autapomorphic Trap’. Denisia 4:67–82Google Scholar
  7. Chong JH, Oetting RD (2007) Intraguild predation and interference by the mealybug predator Cryptolaemus montrouzieri on the parasitoid Leptomastix dactylopii. Biocontrol Sci Technol 17:933–944CrossRefGoogle Scholar
  8. Clausen CP (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. United States Department of Agriculture, Washington, USAGoogle Scholar
  9. Cock MJW (2013) Risks of non-target impact versus stakeholder benefits in classical biological control of arthropods: selected case studies from developing countries. In: van Driesche RG (ed) Proceedings of the international symposium on biological control of arthropods, Honolulu, Hawaii, United States Department of Agriculture, Forest Service, Morgantown, WV, USA, 14–18 Jan 2002, FHTET-2003–05, pp 25–33Google Scholar
  10. De Clercq P (2002) Dark clouds and their silver linings: exotic generalist predators in augmentative biological control. Neotrop Entomol 31:169–176CrossRefGoogle Scholar
  11. De Clercq P, Bonte M, van Speybroeck K, Bolckmans K, Deforce K (2005) Development and reproduction of Adalia bipunctata (Coleoptera: Coccinellidae) on eggs of Ephestia kuehniella (Lepidoptera: Phycitidae) and pollen. Pest Manag Sci 61:1129–1132PubMedCrossRefGoogle Scholar
  12. De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. Biocontrol 56:681–698CrossRefGoogle Scholar
  13. Ehlers RU (2011) Regulation of biocontrol agents in Europe. Springer, Dordrecht, The NetherlandsCrossRefGoogle Scholar
  14. Finlay-Doney M, Walter GH (2012a) Behavioural responses to specific prey and host plant species by a generalist predatory coccinellid (Cryptolaemus montrouzieri Mulsant). Biol Control 63:270–278CrossRefGoogle Scholar
  15. Finlay-Doney M, Walter GH (2012b) The conceptual and practical implications of interpreting diet breath mechanistically in generalist predatory insects. Biol J Linn Soc 107:737–763CrossRefGoogle Scholar
  16. Fisher TW (1963) Mass culture of Cryptolaemus and Leptomastix: natural enemies of the citrus mealybug. California Agricultural experiment station, Berkeley, USAGoogle Scholar
  17. Grenier S, De Clercq P (2003) Comparison of artificially versus naturally reared natural enemies and their potential for use in biological control. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI Publishing, Wallingford, UK, pp 115–131Google Scholar
  18. Hatherly IS, Pedersen BP, Bale JS (2009) Effect of host plant, prey species and intergenerational changes on the prey preferences of the predatory mirid Macrolophus caliginosus. BioControl 54:35–45CrossRefGoogle Scholar
  19. Hodek I, Honěk A (1996) Ecology of Coccinellidae. Kluwer, Dordrecht, The NetherlandsCrossRefGoogle Scholar
  20. Hodek I, Honĕk A (2009) Scale insects, mealybugs, whiteflies and psyllids (Hemiptera: Sternorrhyncha) as prey for ladybirds. Biol Control 51:232–243CrossRefGoogle Scholar
  21. Inc SPSS (2009) Guide to data analysis. SPSS Inc, Chicago, USAGoogle Scholar
  22. Kairo MTK, Paraiso O, Gautam RD, Peterkin DD (2012) Cryptolaemus montrouzieri (Mulsant) (Coccinellidae: Scymninae): a review of biology, ecology, and use in biological control with particular reference to potential impact on non-target organisms. CAB Rev 8:1–20Google Scholar
  23. Kaur H, Virk J (2012) Feeding potential of Cryptolaemus montrouzieri against the mealybug Phenacoccus solenopsis. Phytoparasitica 40:131–136CrossRefGoogle Scholar
  24. Kuhlmann U, Schaffner U, Mason PG (2006) Selection of non-target species for host-specificity testing. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Wallingford, UK, pp 15–37CrossRefGoogle Scholar
  25. Lefcheck JS, Whalen MA, Davenport TM, Stone JP, Duffy JE (2013) Physiological effects of diet mixing on consumer fitness: a meta-analysis. Ecol 94:565–572CrossRefGoogle Scholar
  26. Londsdale WM, Briese DT, Cullen JM (2001) Risk analysis and weed biological control. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, UK, pp 185–210Google Scholar
  27. Loomans AJM, van Lenteren JC (2005) Tools for environmental risk assessment of invertebrate biological control agents: a full and quick scan method. In: Hoddle MS (ed) Second international symposium on biological control of arthropods, Davos, Switzerland, USA, 12–16 Sept, United States Department of Agriculture, Forest Service, Washington, USA, pp 611–619Google Scholar
  28. Maes S, Antoons T, Grégoire JC, De Clercq P (2014) A semi-artificial rearing system for the specialist predatory ladybird Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae). BioControl. doi: 10.1007/s10526-014-9585-8 Google Scholar
  29. Malais MH, Ravensberg WJ (2002) Kennen en herkennen: levenswijzen van kasplagen en hun natuurlijke vijanden. Reed Business Information, Doetinchem, The NetherlandsGoogle Scholar
  30. Manners AG, Palmer WA, Burgos A, McCarthy J, Walter GH (2011) Relative host plant species use by the lantana biological control agent Aconophora compressa (Membracidae) across its native and introduced ranges. Biol Cont 58:262–270CrossRefGoogle Scholar
  31. McCullagh P, Nelder J (1989) Generalized linear models. Chapmann and Hall, London, UKCrossRefGoogle Scholar
  32. Michaud JP (2005) On the assessment of prey suitability in aphidophagous Coccinellidae. Eur J Entomol 102:385–390CrossRefGoogle Scholar
  33. Muştu M, Kilinçer N, Ulgentürk S, Kaydan MB (2008) Feeding behaviour of Cryptolaemus montrouzieri on mealybugs parasitized by Anagyrus pseudococci. Phytoparasitica 36:360–367CrossRefGoogle Scholar
  34. Roy H, Migeon A (2010) Ladybeetles (Coccinellidae). In: Roques A, Kenis M, Lees D, Lopez-Vaamonde C, Rabitsch W, Rasplus J-Y, Roy D (eds) Alien terrestrial arthropods of Europe. BioRisk 4: 293–313Google Scholar
  35. Sands DPA, van Driesche RG (2000) Evaluating the host range of agents for biological control of arthropods: rationale, methodology and interpretation. In: van Driesche RG, Heard TA, McClay AS, Reardon R (eds) Host specificity testing of exotic biological control agents: the biological basis for improvement in safety. Proceedings of the international symposium on biological control of weeds, Montana, USA, 4–11 July, United States Department of Agriculture, Forest Service, Washington, USA, pp 69–83Google Scholar
  36. Ślipiński SA (2007) Australian ladybird beetles (Coleoptera: Coccinellidae): their biology and classification. Australian Biological Resources Study, Canberra, AustraliaGoogle Scholar
  37. van Driesche RG, Murray TJ (2004a) Parameters used in laboratory host range tests. In: van Driesche RG, Murray TJ, Reardon R (eds) Assessing host ranges of parasitoids and predators used for classical biological control: a guide to best practice. Forest Health Technology Enterprise Team, Morgantown, USA, pp 56–67Google Scholar
  38. van Driesche RG, Murray TJ (2004b) Overview of testing schemes and designs used to estimate host ranges. In: van Driesche RG, Murray TJ, Reardon R (eds) Assessing host ranges of parasitoids and predators used for classical biological control: a guide to best practice. Forest Health Technology Enterprise Team, Morgantown, pp 68–89Google Scholar
  39. van Lenteren JC, Loomans AJM (2006) Environmental risk assessment: methods for comprehensive evaluation and quick scan. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. Methods and risk assessment. CABI Publishing, Wallingford, UK, pp 254–272CrossRefGoogle Scholar
  40. van Lenteren JC, Woets J (1988) Biological and integrated pest control in greenhouses. Annu Rev Entomol 33:239–269CrossRefGoogle Scholar
  41. van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, van Rijn PCJ, Thomas MB, Tommasini MG, Zeng QQ (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38CrossRefGoogle Scholar
  42. van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006a) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634PubMedCrossRefGoogle Scholar
  43. van Lenteren JC, Cock MJW, Hoffmeister TS, Sands DPA (2006b) Host specificity in arthropod biological control, methods for testing and interpretation of data. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. Methods and risk assessment. CABI Publishing, Wallingford, UK, pp 38–63CrossRefGoogle Scholar
  44. Vanhaecke M, Degheele D (1980) Electrophoretic characterization of the haemolymph proteins, glyco- and lipoproteins of Galleria mellonella, Plodia interpunctella and Ephestia kuehniella. Meded Fac Landbouwwet, Rijksuniv. Gent 45:1287–1297Google Scholar
  45. Wapshere AJ (1974) A strategy for evaluating of organisms for biological weed control. Ann Appl Biol 77:201–211CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2014

Authors and Affiliations

  • Sara Maes
    • 1
  • Jean-Claude Grégoire
    • 2
  • Patrick De Clercq
    • 1
  1. 1.Laboratory of Agrozoology, Department of Crop ProtectionGhent UniversityGhentBelgium
  2. 2.Biological Control and Spatial Ecology LabULBBrusselsBelgium

Personalised recommendations