Multitrophic Interactions: The Entomovector Technology

  • Guy Smagghe
  • Veerle Mommaerts
  • Heikki Hokkanen
  • Ingeborg Menzler-Hokkanen
Chapter
First Online:
Part of the Progress in Biological Control book series (PIBC, volume 14)

Abstract

The entomovector technology (Hokkanen and Menzler-Hokkanen 2007; Mommaerts and Smagghe 2011) utilizes insects as vectors of biological control agents for targeted precision biocontrol towards plant pests and diseases, providing an intriguing example of multitrophic interactions. As the insect vector normally is a pollinator of the crop plant, it adds a further dimension to these interactions. The technology depends on bee management, manipulation of bee behaviour, components of the cropping system, and on the plant-pathogen-vector-antagonist-system. We investigate in this chapter how to exploit and support the natural ecological functions of biocontrol and pollination, and enhance these via innovative management. Recent systematic developments of the entomovector technology are described, with focus on the component technologies such as the dispensers and carrier substances (see Mommaerts and Smagghe 2011; Mommaerts et al. 2011; Hokkanen et al. 2012). With functioning dispensers and improved, new microbiological control agents (MCA) available, excellent results have been obtained, and will be described in two case studies. The first involves open field studies conducted in Finland with honey bees (Apis mellifera Linnaeus (Hymenoptera: Apidae)) as the vector of “Prestop-Mix”, containing Gliocladium catenulatum J1446 (Hypocreales, Bionectriaceae), to control Botrytis cinerea Pers.: Fr. (Helotiales: Sclerotiniaceae) in strawberries, and the second describes the efficiency of bumble bees (Bombus terrestris Linnaeus (Hymenoptera: Apidae)) to vector the commercial product “Prestop-Mix” to control B. cinerea in strawberries in the greenhouse.

Keywords

Biological Control Biological Control Agent Predatory Mite Sweet Pepper Grey Mould 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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Notes

Acknowledgements

The authors acknowledge support for their research by the Fund for Scientific Research-Flanders (FWO-Vlaanderen), the Flemish agency for Innovation by Science and Technology (IWT-Vlaanderen), the Special Research Funds of Ghent University and of VUB, NordForsk grant 70066 (Entomovector technology), NordForsk Project no. 45941 (BICOPOLL-NET), and CORE-Organic II project “BICOPOLL” in an ERA-NET funded by the European Commission’s 7th Framework Program.

References

  1. AAFC (2009) Crop profile for strawberry in Canada. Agriculture and Agri-Food Canada. Available at http://dsp-psd.pwgsc.gc.ca/collection_2009/agr/A118-10-17-2005E.pdf. Accessed on 10 Feb 2011
  2. Albano S, Chagon M, de Oliveira D, Houle E, Thibodeau PO, Mexia A (2009) Effectiveness of Apis mellifera and Bombus impatiens as dispensers of the Rootshield® biofungicide (Trichoderma harzianum, strain T-22) in a strawberry crop. Hell Plant Prot J 2:57–66Google Scholar
  3. Alexandrova M, Bazzi C, Lameri P (2002) Bacillus subtilis strain BS-F3: colonisation of pear organs and its action as a biocontrol agent. Acta Hortic 590:291–297Google Scholar
  4. Al-mazra’awi MS, Shipp JL, Broadbent AB, Kevan PG (2006a) Dissemination of Beauveria bassiana by honey bees (Hymenoptera: Apidae) for control tarnished plant bug (Hemiptera: Miridae) on canola. Biol Control 35:1569–1577Google Scholar
  5. Al-mazra’awi MS, Shipp JL, Broadbent AB, Kevan PG (2006b) Biological control of Lygus lineolaris (Hemiptera: Miridae) and Frankiniella occidentalis (Thysanoptera: Thripidae) by Bombus impatiens (Hymenoptera: Apidae) vectored Beauveria bassiana in greenhouse sweet pepper. Biol Control 37:89–97CrossRefGoogle Scholar
  6. Al-mazra’awi MS, Kevan PG, Shipp L (2007) Development of Beauveria bassiana dry formulation for vectoring by honey bees Apis mellifera (Hymenoptera: Apidae) to the flowers of crops for pest control. Biocontrol Sci Technol 17:733–741CrossRefGoogle Scholar
  7. Beever RE, Weeds PL (2004) Taxonomy and genetic variation of Botrytis and Botryotinia. In: Elad Y, Williamson B, Tudzynski B, Delen N (eds) Botrytis: biology, pathology and control. Kluwer Academic Publishers, Dordrecht/Boston/London, pp 29–52Google Scholar
  8. Bilu A, Dag A, Elad Y, Shafir S (2004) Honey bee dispersal of biocontrol agents: an evaluation of dispensing devices. Biocontrol Sci Technol 14:607–617CrossRefGoogle Scholar
  9. Bosch J, Kemp WP (2002) Developing and establishing bee species as crop pollinators: the example of Osmia spp. (Hymenoptera: Megachilidae) and fruit trees. Bull Entomol Res 92:3–16PubMedGoogle Scholar
  10. Butt TM, Carreck NL, Ibrahim L, Williams IH (1998) Honey bee-mediated infection of pollen beetle (Meligethes aeneus Fab.) by the insect-pathogenic fungus, Metarhizium anisopliae. Biocontrol Sci Technol 8:533–538CrossRefGoogle Scholar
  11. Carreck NL, Butt TM, Clark SJ, Ibrahim L, Isger EA, Pell JK, Williams IH (2007) Honey bees can disseminate a microbial control agent to more than one inflorescence pest of oilseed rape. Biocontrol Sci Technol 17:179–191CrossRefGoogle Scholar
  12. Christensen L (2006) Practical use of biological control of pest and diseases in Danish glasshouses - bottlnecks and challenges. In: Hansen LS, Enkegaard A, Steenberg T, Ravnskov S, Larsen J (eds) Proceedings of the International Workshop “Implementation of Biocontrol in Practice in Temperate Regions - Present and Near Future”. DIAS report Plant Production 119:169–171Google Scholar
  13. Cohen AC, Nordlund DA, Smith RA (1999) Mass rearing of entomophagous insects and predaceous mites: are the bottlenecks biological, engineering, economic, or cultural? Biocontrol News Info 20(3):85N–90NGoogle Scholar
  14. Cribb DM, Hand DW (1993) A comparative study of the effects of using the honeybee as a pollinating agent of glasshouse tomato. J Hortic Sci 68:79–88Google Scholar
  15. Dag A, Weinbaum SA, Thorp R, Eiskowitch D (2000) Evaluation of pollen dispensers (‘inserts’) effect on fruit set and yield in almond. J Apic Res 39:117–123Google Scholar
  16. Dedej S, Delaplane KS, Scherm H (2004) Effectiveness of honey bees in delivering the biocontrol agent Bacillus subtilis to blueberry flowers to suppress mummy berry disease. Biol Control 31:422–427CrossRefGoogle Scholar
  17. Elad Y, Freeman S (2002) Biological control of fungal plant pathogens. In: Kempken F (ed) The Mycota, a comprehensive treatise on fungi as experimental systems for basic and applied research. Springer, HeidelbergGoogle Scholar
  18. Escande AR, Laich FS, Pedraza MV (2002) Field testing of honeybee-dispersed Trichoderma spp. to manage sunflower head rot (Sclerotinia sclerotiorum). Plant Pathol 51:346–351CrossRefGoogle Scholar
  19. FAO (2011) FAOSTAT agricultural production statistics. Available at http://faostat.fao.org/site/567/ and at http://faostat.fao.org/site/339/. Accessed on 10 Feb 2011
  20. Farina WM, Gruter C, Acosta L, Cabe SMC (2007) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissensch 94:55–60CrossRefGoogle Scholar
  21. Forrest J, Thomson JD (2009) Background complexity affects colour preference in bumblebees. Naturwissensch 96:921–925CrossRefGoogle Scholar
  22. Frost & Sullivan (2001) European biopesticides market. Available at http://www.frost.com. Accessed 15 Apr 2005
  23. Gelernter WD, Lomer CJ (2000) Success in biological control of above-ground insects by pathogens. In: Gurr G, Wratten SD (eds) Biological control: measures of success. Kluwer Academic Publishers, DordrechtGoogle Scholar
  24. Gil M (2010) Reward expectations in honeybees. Commun Integr Biol 3:95–100PubMedCrossRefGoogle Scholar
  25. Goulson D (2010) Bumblebees behaviour, ecology and conservation. Oxford University Press, New York, pp 317Google Scholar
  26. Gross HR, Hamm JJ, Carpenter JE (1994) Design and application of a hive-mounted device that uses honey bees (Hymenoptera: Apidae) to disseminate Heliothis nuclear polyhedrosis virus. Biol Control 23:492–501Google Scholar
  27. Guerra-Sanz JM (2008) Crop pollination in greenhouses. In: James RR, Pitts-Singer T (eds) Bee pollination in agriculture ecosystems. Oxford University Press, New YorkGoogle Scholar
  28. Hjeljord LG, Stensvand A, Tronsmo A (2000) Effect of temperature and nutrient stress on the capacity of commercial Trichoderma products to control Botrytis cinerea and Mucor piriformis in greenhouse strawberries. Biol Control 19:149–160CrossRefGoogle Scholar
  29. Hokkanen HMT, Menzler-Hokkanen I (2007) Use of honeybees in the biological control of plant diseases. Entomol Res 37(suppl 1):A62–A63Google Scholar
  30. Hokkanen HMT, Menzler-Hokkanen I (2009) Successful use of honey bees for grey mould biocontrol on strawberries and raspberries in Finland. Apidologie 40:659Google Scholar
  31. Hokkanen HMT, Menzler-Hokkanen I, Mustalahti A-M (2012) Honey bees (Apis mellifera) for precision biocontrol of grey mould (Botrytis cinerea) with Gliocladium catenulatum on strawberries and raspberries in Finland. Arthropod-Plant Interactions (submitted)Google Scholar
  32. IPMCenters (2011) Crop profile for strawberries in Louisiana. Available at http://www.ipmcenters.org/cropprofiles/docs/LAstrawberries.pdf. Accessed on 10 Feb 2011
  33. Israel MS, Boland GJ (1993) Influence of formulation on efficacy of honey bees to transmit biological controls for management of Sclerotinia stem rot of canola. Can J Plant Pathol 14:244Google Scholar
  34. Johnson KB, Stockwell VO, Burgett DM, Sugar D, Loper JE (1993a) Dispersal of Erwinia amylovora and Pseudomonas fluorescens by honeybees from hives to apple and pear blossoms. Phytopathology 83:478–484CrossRefGoogle Scholar
  35. Johnson KB, Stockwell VO, Mclaughlin RJ (1993b) Effect of antagonistic bacteria on establishment of honey bee-dispersed Erwinia amylovora in pear blossoms and on fire blight control. Phytopathology 83:995–1002CrossRefGoogle Scholar
  36. Jyoti JL, Brewer GJ (1999) Honeybees (Hymenoptera: Apidae) as vector of Bacillus thuringiensis for control of branded sunflower moth (Lepidoptera: Tortricidae). Environ Entomol 28:1172–1176Google Scholar
  37. Kapongo JP, Shipp L, Kevan P (2008a) Optimal concentration of Beauveria bassiana vectored by bumble bees in relation to pest and bee mortality in greenhouse tomato and sweet pepper. Biocontrol 53:797–812CrossRefGoogle Scholar
  38. Kapongo JP, Shipp L, Kevan P, Sutton JC (2008b) Co-vectoring of Beauveria bassiana and Clonostachys rosea by bumblebees (Bombus impatiens) for control of insect pests and suppression of grey mould in greenhouse tomato and sweet pepper. Biol Control 46:508–514CrossRefGoogle Scholar
  39. Kevan PG, Kapongo J-P, Al-mazra’awi M, Shipp L (2008) Honey bees, bumble bees and biocontrol. In: James RR, Pitts-Singer T (eds) Bee pollination in agriculture ecosystems. Oxford University Press, New YorkGoogle Scholar
  40. Kovach J, Petzoldt R, Harman GE (2000) Use of honeybees and bumble bees to disseminate Trichoderma harzianum 1295–22 to strawberries for Botrytis control. Biol Control 18:235–242CrossRefGoogle Scholar
  41. Lunau K, Unseld K, Wolter F (2009) Visual detection of diminutive floral guides in the bumblebee Bombus terrestris and in the honeybee Apis mellifera. J Comp Physiol 195A:1121–1130CrossRefGoogle Scholar
  42. Maccagnani B, Mocioni M, Gullino ML, Ladurner E (1999) Application of Trichoderma harzianum by using Apis mellifera as a vector for the control of grey mold of strawberry: first results. IOBC Bull 22:161–164Google Scholar
  43. Maccagnani B, Mocioni M, Ladurner E, Gullino ML, Maini S (2005) Investigation of hive-mounted devices for the dissemination of microbiological preparations by Bombus terrestris. Bull Insectol 58:3–8Google Scholar
  44. Maccagnani BBC, Biondi E, Tesoriero D, Maini S (2006) Potential of Osmia cornuta as a carrier of antagonist bacteria in biological control of fire blight: a comparison with Apis mellifera. Acta Hort (ISHS) 704:379–386Google Scholar
  45. Mertley JC, Mackenzie SJ, Legard DE (2002) Timing of fungicide applications for Botrytis cinerea based on development stage of strawberry flowers and fruit. Plant Dis 86:1019–1024CrossRefGoogle Scholar
  46. Molet M, Chittka L, Raine NE (2009) How floral odours are learned inside the bumblebee (Bombus terrestris) nest? Naturwissensch 96:213–219CrossRefGoogle Scholar
  47. Mommaerts V, Smagghe G (2011) Entomovectoring in plant protection. Arthropod-Plant Interact 5:81–95CrossRefGoogle Scholar
  48. Mommaerts V, Put K, Vandeven J, Jans K, Sterk G, Hoffmann L, Smagghe G (2010) Development of a new dispenser for bumblebees and evaluation to disseminate microbiological control agents in strawberry in the greenhouse. Pest Manag Sci 66:1199–1207PubMedCrossRefGoogle Scholar
  49. Mommaerts V, Kurt P, Smagghe G (2011) Bombus terrestris as pollinator-and-vector to suppress Botrytis cinerea in greenhouse strawberry. Pest Manag Sci 67:1069–1075Google Scholar
  50. Moscardi F (1999) Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289PubMedCrossRefGoogle Scholar
  51. Ngugi HK, Scherm H, Lehman JS (2002) Relationship between blueberry flower age, pollination and conidal infection by Monilinia vaccinii-corymbosi. Ecol Popul Biol 92:1104–1109Google Scholar
  52. Nilsson U, Gripwall E (1999) Influence of application technique on the viability of the biological control agents Verticillium lecanii and Stenernema feltiae. Crop Prot 18:53–59CrossRefGoogle Scholar
  53. Noma T, Strickler K (2000) Effects of Beauveria bassiana on Lygus hesperus (Hemiptera: Miridae) feeding and oviposition. Environ Entomol 29:394–402CrossRefGoogle Scholar
  54. Oh CS, Beer SV (2005) Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol Lett 253:185–192PubMedCrossRefGoogle Scholar
  55. Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:401–415CrossRefGoogle Scholar
  56. Peng G, Sutton JC, Kevan PG (1992) Effectiveness of honeybees for applying the biocontrol agent Gliocladium rosea to strawberry flowers to suppress Botrytis cinerea. Can J Plant Pathol 14:117–129CrossRefGoogle Scholar
  57. Pettis JS, Kochansky J, Feldlaufer MF (2004) Larval Apis mellifera L. (Hymenoptera: Apidae) mortality after topical application of antibiotics and dusts. J Econ Entomol 97:171–176PubMedCrossRefGoogle Scholar
  58. Pilkington LJ, Messelink G, van Lenteren JC, Le Mottee K (2010) Protected biological control – biological pest management in the greenhouse industry. Biol Control 52:216–220CrossRefGoogle Scholar
  59. Prokkola S, Kivijärvi P (2007) Effect of biological sprays on the incidence of grey mould, fruit yield and fruit quality in organic strawberry production. Agric Food Sci 16:25–33CrossRefGoogle Scholar
  60. Raine NE, Chittka L (2007) The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris. PLoS One 2(6):e556. doi: 10.1371/journal.pone.0000556 PubMedCrossRefGoogle Scholar
  61. Rands SA, Whitney HM (2008) Floral temperature and optimal foraging: is heat a feasible floral reward for pollinators? PLoS One 3(4):e2007. doi: 10.1371/journal.pone.0002007 PubMedCrossRefGoogle Scholar
  62. Ravensberg W (2011) A roadmap to the successful development and commercialization of microbial pest control products for control of arthropods, vol 10, Progress in biological control. Springer, Zoetermeer, 383 pCrossRefGoogle Scholar
  63. Scherm H, Ngugi HK, Savelle AT, Edwards JR (2004) Biological control of infection of blueberry flowers caused by Monilinia vaccinii-corymbosi. Biol Control 29:199–206CrossRefGoogle Scholar
  64. Shafir S, Dag A, Bilu A, Abu-Toamy M, Elad Y (2006) Honeybee dispersal of the biocontrol agent and Trichoderma harzianum T39: effectiveness in suppressing Botrytis cinerea on strawberry under field conditions. Eur J Plant Pathol 116:119–128CrossRefGoogle Scholar
  65. Shinners TC, Olson AR (1996) The gynoecial infection pathway of Monilinia vaccinii-corymbosi in lowbush blueberry (Vaccinium angustifolium). Can J Plant Sci 76:493–497CrossRefGoogle Scholar
  66. Sigsgaard L (2006) Biological control of arthropod pests in outdoor crops – the new challenge. DIAS report Plant Production 119, pp 153–168Google Scholar
  67. Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and color affect search time and flight behaviour. Proc Natl Acad Sci USA 98:3898–3903PubMedCrossRefGoogle Scholar
  68. Stout JC, Goulson D (2002) The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behav Ecol Sociobiol 52:239–246CrossRefGoogle Scholar
  69. Strømeng GM (2008) Aspects of the biology of Botrytis cinerea in strawberry (Fragaria x ananassa) and alternative methods for disease control. Philosophiae Doctor (PhD) thesis 2008, pp 56Google Scholar
  70. Thomson SV, Hansen DR, Flint KM, Vandenberg JD (1992) Dissemination of bacteria antagonistic to Erwinia amylovora by honey bees. Plant Dis 76:1052–1056CrossRefGoogle Scholar
  71. Törmälä T (1995) Economics of biocontrol agents: an industrial view. In: Hokkanen HMT, Lynch JM (eds) Biological control: benefits and risks. Cambridge University Press, Cambridge, pp 277–282CrossRefGoogle Scholar
  72. van der Blom J, Robledo A, Torres S, Sánchez JA (2009) Consequences of the wide scale implementation of biological control in greenhouse horticulture in Almeria. Spain. IOBC/WPRS Bull 49:9–13Google Scholar
  73. van Lenteren JC (ed) (2008) Internet book of biological control, 5th edn. IOBC, Wageningen, www.IOBC-Global.orgGoogle Scholar
  74. Vanneste JL (1996) Honey bees and epiphytic bacteria to control fire blight, a bacterial disease of apple and pear. Biocont News Info 17:67N–78NGoogle Scholar
  75. Vicens N, Bosch J (2000) Pollinating efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on ‘Red Delicious’ apple. Environ Entomol 29:235–240CrossRefGoogle Scholar
  76. Whitney HM, Dyer A, Chittka L, Rands SA, Glover BJ (2008) The interaction of temperature and sucrose concentration on foraging preferences in bumblebees. Naturwissensch 95:845–850CrossRefGoogle Scholar
  77. Williamson B, Tudzynski B, Tudzynski P, Van Kan JAL (2007) Botrytis cinerea: the cause of grey mold disease. Mol Plant Pathol 8:561–580PubMedCrossRefGoogle Scholar
  78. Wilson M, Lindow SE (1993) Interactions between the biological control agent Pseudomonas fluorescens A506 and Erwinia amylovora in pear blossoms. Phytopathology 83:117–123CrossRefGoogle Scholar
  79. Wilson M, Epton HAS, Sigee DC (1992) Interactions between Erwinia herbicola and E. amylovora on the stigma of hawthorn blossoms. Phytopathology 82:914–918CrossRefGoogle Scholar
  80. Wolf S, Moritz RFA (2008) Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae). Apidologie 39:419–427CrossRefGoogle Scholar
  81. Yu H, Sutton JC (1997) Effectiveness of bumblebees and honeybees for delivering inoculum of Gliocladium roseum to raspberry flowers to control Botrytis cinerea. Biol Control 10:113–122CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Guy Smagghe
    • 1
  • Veerle Mommaerts
    • 1
    • 2
  • Heikki Hokkanen
    • 3
  • Ingeborg Menzler-Hokkanen
    • 3
  1. 1.Department of Crop Protection, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium
  2. 2.Department of Biology, Faculty of Science and Bio-engineering SciencesVrije Universiteit BrusselBrusselsBelgium
  3. 3.Department of Agricultural SciencesUniversity of HelsinkiHelsinkiFinland

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