ANRV330-EN53-07 ARI 2 November 2007 16:8 Microbial Control of Insect Pests in Temperate Orchard Systems: Potential for ∗ Incorporation into IPM Lawrence A. Lacey1 and David I. Shapiro-Ilan2 1USDA-ARS, Yakima Agriculture Research Laboratory, Wapato, Washington 98908; email: [email protected] 2USDA-ARS, SE Fruit and Tree Nut Research Laboratory, Byron, Georgia 31008; email: [email protected] Annu. Rev. Entomol. 2008. 53:121–44 Key Words First published online as a Review in Advance on Bacillus thuringiensis, entomopathogenic nematodes, fungi, September 5, 2007 granulovirus, tree fruit, nut crops The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: Because of their selectivity and safety, microbial control agents 10.1146/annurev.ento.53.103106.093419 (MCAs) appear to be ready-made components of integrated pest by Dr. David Shapiro-Ilan on 12/13/07. For personal use only. Copyright c 2008 by Annual Reviews. management (IPM) systems that do not pose a threat to applica- All rights reserved tors or the environment and allow other natural enemies to func- 0066-4170/08/0107-0121$20.00 tion. Control of several orchard pest insects using MCAs, including ∗ The U.S. Government has the right to retain a viruses, Bacillus thuringiensis, fungi, and entomopathogenic nema- Annu. Rev. Entomol. 2008.53:121-144. Downloaded from arjournals.annualreviews.org nonexclusive, royalty-free license in and to any todes (EPNs), have been demonstrated in apple, pear, stone fruits, copyright covering this paper. citrus, and several nut crops. B. thuringiensis is the most used MCA for control of lepidopteran orchard pests. Significant use of EPNs in citrus for control of root weevils is also reported. The granulovirus of codling moth is used increasingly in apple and pear by organic growers, with interest also shown by conventional growers. Although some success has been achieved, in most orchard systems MCAs ac- count for a relatively small proportion of the pest control tactics employed, and in some systems they are not used at all. Research toward improving MCA efficacy and economic competitiveness is required to enhance the role of MCAs in IPM. 121 ANRV330-EN53-07 ARI 2 November 2007 16:8 INTRODUCTION opment (78, 120). They are reported from Lepidoptera, Coleoptera, Diptera, and Hy- The primary means of control of arthro- menoptera (sawflies), but their use in orchards IPM: integrated pod pests of temperate tree fruits and nuts is exclusively for control of lepidopteran pests. pest management is through the application of broad-spectrum Two distinct groups, nucleopolyhedroviruses Entomopathogen: insecticides. While such interventions are ca- and granuloviruses, have been used for experi- a microorganism or pable of rapidly killing a range of pests, over- mental and practical control of a limited num- nematode capable of reliance on chemical pesticides has generated producing disease in ber of orchard pests. The specificity of viruses a panoply of problems including safety risks, an insect used for control of lepidopteran orchard pests outbreaks of secondary pests normally held MCA: microbial is well documented (68). The narrow host in check by natural enemies, environmental control agent ranges of most entomopathogenic viruses can contamination, decrease in biodiversity, and be both a limitation and advantage depending insecticide resistance. In our current climate on the suite of arthropod pests in a particular of increased awareness of the sensitivity of orchard ecosystem and on the controlling ef- our environment, among both the scientific fects exerted by predators and parasitoids and community and the general public, the devel- other alternatives to broad-spectrum insecti- opment of environmentally safer methods of cides. Generally, sensitivity to solar degrada- insect control is desirable. Tightened registra- tion necessitates reapplication of virus prepa- tion procedures around the world will likely rations at fairly short intervals, particularly if result in a decreased availability of a number of the host is multivoltine and if pest population broad-spectrum pesticides, creating new op- pressure is high (10). Shading and microhabi- portunities for alternative methods (including tats on the host plant and in the environment microbials). An integrated pest management can protect some viruses from solar degrada- (IPM) strategy, in which natural enemies of tion and enable long-term persistence (30). pest arthropods and other alternative mea- sures play significant roles in crop protec- tion, will minimize negative environmental BACTERIA impacts and other deleterious effects due to Various spore-forming and nonspore- insecticide usage while providing a more sus- forming bacteria are pathogens of insects, tainable approach to pest control. Several en- but only has been used in tomopathogens (viruses, bacteria, fungi, and Bacillus thuringiensis orchards. has been employed nematodes) offer effective means of micro- B. thuringiensis to control a multitude of insects in organic bial control that can be combined with other by Dr. David Shapiro-Ilan on 12/13/07. For personal use only. and conventional agriculture, forestry, and tactics such as mating disruption and the use public health (18). Its safety to pesticide of reduced-risk pesticides. In addition, mi- applicators, the food supply, beneficial or- crobial control agents (MCAs) are safe for ganisms, and the environment is thoroughly Annu. Rev. Entomol. 2008.53:121-144. Downloaded from arjournals.annualreviews.org the environment, beneficial insects, applica- documented (97). A variety of tors, and the food supply, and they can be ap- B. thuringiensis formulations are commercially produced in plied just prior to harvest (88). We provide several countries with insecticidal activity an overview of microbial control in temperate for species of Lepidoptera, Coleoptera, and orchards designed to set the stage for incorpo- Diptera (18, 57), but only those formulations rating MCAs into IPM programs for orchard with activity against lepidopteran pests systems. are used in orchards (92). The insecticidal activity of B. thuringiensis is due to the crystal VIRUSES protein toxins contained in the parasporal Several major groups of viruses infect insects inclusions that are produced at the time and mites, but baculoviruses have received of sporulation (35). These toxins basically the most attention and commercial devel- function as stomach poisons and kill the 122 Lacey · Shapiro-Ilan ANRV330-EN53-07 ARI 2 November 2007 16:8 insect by disrupting osmotic balance in the todes (EPNs), which consist of the fami- midgut epithelium. Damage to the midgut lies Steinernematidae and Heterorhabditidae epithelium results in cessation of feeding (59, 66, 182). EPNs kill their hosts with the Epizootic: an and gut paralysis and ultimately death. B. aid of bacteria carried in the nematode in- outbreak of disease thuringiensis products are made up primarily testine (steinernematids are associated with in which there is an of spores and toxins (57), thus differing from Xenorhabdus spp. and heterorhabditids are as- unusually large most other MCA products (e.g., nematodes, sociated with Photorhabdus spp.) (1, 22). De- number of cases and fungi, and viruses), which contain the entire tailed aspects of the biology and life cycle high morbidity organisms. More detailed descriptions of B. of EPN are reviewed elsewhere (1, 86). The EPN: entomopathogenic thuringiensis, its toxins, and their mode of safety of EPNs to humans and other nontar- nematode action are presented by Schnepf et al. (144) gets has been well recognized and led to their and Garczynski & Siegel (57). exemption from U.S. EPA pesticide registra- CM: codling moth tion (4). EPNs can be mass produced in vivo FUNGI or in vitro and applied using various stan- dard agricultural equipment (161, 163). Be- A diverse spectrum of fungi is reported from cause of their sensitivity to UV degradation insects and mites (63, 195). Some species in and desiccation, EPNs are most suitable for the Entomophthorales (e.g., Neozygites fre- application to soil or cryptic (protected) habi- senii, Entomophaga maimaiga) and Hypocre- tats (163). Most insect targets are in the or- ales (e.g., Lecanicillium spp., Aschersonia spp., ders Coleoptera and Lepidoptera, but exam- and Hirsutella spp.) produce epizootics in ples may also be found among other orders pest populations that often lower pest den- such as Blattodea, Diptera, Hymenoptera, sities to levels that are not harmful to the Orthoptera, Siphonaptera, and Thysanoptera crop (181). Commercial development of en- (66). tomopathogenic fungi has been confined to species in the Hypocreales, most no- tably Lecanicillium spp., Beauveria bassiana, MICROBIAL CONTROL Metarhizium anisopliae, and Paecilomyces fu- OF ORCHARD PESTS mosoroseus (63). In general, these fungi are in- undatively applied to bring about a rapid re- Pome Fruits duction in the pest population. Because fungi Several varieties of pome fruits, including ap- gain access to the host through the cuticle, ple, crab apple, pear, and quince, are grown they are the principal MCAs of sucking insects by Dr. David Shapiro-Ilan on 12/13/07. For personal use only. in temperate climates. Apple and pear are the (Hemiptera, e.g., aphids and whiteflies) and major pome fruit crops in the temperate cli- control a variety of insects in other orders such mate zones. A rich diversity of insects and as Coleoptera, Lepidoptera, and Orthoptera mites attack