Biocontrol of Pests of Apples and Pears in Northern and Central Europe: 1. Microbial Agents and Nematodes

Abstract
The viral, bacterial, fungal and nematode pathogens of arthropod pests of apple and pear in northern and central Europe and their use as biocontrol agents are reviewed. Baculoviruses are important viral pathogens of several lepidopterous pests of apple and pear but other viral pathogens have not been investigated in depth and are little known. The granuloviruses of codling moth, Cydia pomonella (CpGV), and to a lesser extent, of the summer fruit tortrix moth, Adoxophyes orana (AoGV), have been researched extensively and are exploited as biological control agents. Commercial development and use has been limited because of their high costs, slow action, short persistence and specificity relative to broad-spectrum pesticides. The widespread development of strains of codling moth multi-resistant to insecticides and the desire to reduce dependence on pesticides have improved the commercial prospects of CpGV and use is likely to increase. The development of a genetically improved egt-strain of CpGV (lacking the ecdysteroid-UDP glucosyl transferase gene) in the UK is a significant breakthrough, though commercialization in the UK may be difficult due to adverse public attitudes to the release of genetically-modified microorganisms. Future research and development approaches include further genetic manipulation of CpGV and AoGV to improve potency, speed of kill and/or persistence, improvement of formulation (to reduce UV light sensitivity) and development of cheaper mass production techniques and possibly in vitro production. A systematic search for baculoviruses and other viruses of apple and pear pests is likely to reveal important new opportunities. The most important bacterial pathogen used as a biological control agent is Bacillus thuringiensis (Bt). However, Bt products currently available have limited effectiveness against many orchard pests due to the pests' cryptic life habits. The HD-1 Bt strain has been investigated and used extensively for control of leaf-rolling tortricid larvae and is widely used, but efficacy is moderate. Advances in biotechnology and genetic engineering provide opportunity for development of Bt strains designed specifically to control orchard pests, but this has not yet been done for commercial reasons. Other research approaches include the evaluation of new Bt products developed for other markets worldwide and the bioassay of strains from Bt collections against specific apple or pear pests. Entomopathogenic fungi provide good opportunity for development as biological control agents of apple and pear pests. The main factor limiting their effectiveness is the requirement for high humidities and moderate temperatures for spore germination and development. For foliar pests, a useful starting point for research might be the control of sucking pests which excrete honeydew (e.g. Cacopsylla sp. or aphids) or those that inhabit protected microenvironments (e.g. Dasineura sp.). Key areas for research are improved formulation, the selection of low temperature-active strains, field evaluation and avoiding possible adverse effects of fungicides. An alternative approach is to examine the exploitation of entomopathogenic fungi in soil, to which many species of entomopathogenic fungi are adapted ecologically. Apple and pear orchards provide long-term stable habitats where populations of entomopathogenic fungi in soil are likely to be large. There are few important soil pests of apple or pear. However, many species spend part of their life in soil, mainly to pupate or overwinter, where they may be targeted by fungal entomopathogenic biocontrol agents. Entomopathogenic nematodes have many attributes which favour them as biological control agents. However, their requirement for surface moisture for survival and movement means there are only limited prospects for using them as biological control agents for foliar pests. As with entomopathogenic fungi, there are better prospects for control of pests that occur in soil. Microbial pathogens and entomopathogenic nematodes are important components of the natural enemy complex of apple and pear orchards and more effort needs to be devoted to fostering them and exploiting them as biocontrol agents in sustainable, biologically-based Integrated Pest Management programmes. They can in many cases be mass produced at low cost by bulk fermentation processes and applied as sprays (as 'biopesticides') and are, at least potentially, ideal biological control agents for many apple or pear pests. Important general characteristics are their comparative environmental and human safety, compatibility with other control strategies in Integrated Pest Management programmes and reproductive capacity. They tend to be effective in a narrower range of environmental conditions than pesticides, but there is considerable potential to improve their effectiveness by improved formulation, strain selection and genetic manipulation. They are often host-specific and thus, offer restricted marketing opportunities, which is a significant barrier to development and commercialisation. Registration procedures and associated fees for microbial agents are a further significant barrier. Such requirements do not apply currently to nematodes.

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