This article was downloaded by: [USDA National Agricultural Library] On: 28 October 2008 Access details: Access Details: [subscription number 790740294] Publisher Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Biocontrol Science and Technology Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713409232
Codling moth granulovirus: a comprehensive review Lawrence A. Lacey a; Donald Thomson b; Charles Vincent c; Steven P. Arthurs d a Yakima Agricultural Research Laboratory, USDA-ARS, Wapato, WA, USA b DJS Consulting Services, Seattle, WA, USA c Centre de recherche et de développement en horticulture, Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, QC, Canada d Department of Entomology and Nematology, University of Florida, IFAS, Mid Florida Research and Education Center, Apopka, FL, USA
First Published on: 13 August 2008
To cite this Article Lacey, Lawrence A., Thomson, Donald, Vincent, Charles and Arthurs, Steven P.(2008)'Codling moth granulovirus: a comprehensive review',Biocontrol Science and Technology,18:7,639 — 663 To link to this Article: DOI: 10.1080/09583150802267046 URL: http://dx.doi.org/10.1080/09583150802267046
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf
This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Biocontrol Science and Technology, Vol. 18, No. 7, 2008, 639 663
REVIEW Codling moth granulovirus: a comprehensive review Lawrence A. Laceya*, Donald Thomsonb, Charles Vincentc and Steven P. Arthursd
aYakima Agricultural Research Laboratory, USDA-ARS, Wapato, WA, USA; bDJS Consulting Services, Seattle, WA, USA; cCentre de recherche et de de´veloppement en horticulture, Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, QC, Canada; dDepartment of Entomology and Nematology, University of Florida, IFAS, Mid Florida Research and Education Center, Apopka, FL, USA (Received 25 March 2008; returned 16 May 2008; accepted 10 June 2008)
Codling moth (CM), Cydia pomonella (L), is regarded as the most serious insect pest of apple worldwide. A variety of problems associated with the traditional use of non- selective insecticides for its control include: untoward environmental effects, insecticide resistance, negative impacts on natural enemies, and safety for pesticide applicators and the food supply. Concerns about these consequences have increased the interest in and development of alternative means for CM control that have little or no impact on humans, beneficial organisms and sensitive ecosystems. An effective and selective alternative to chemical insecticides for CM control is the CM granulovirus (CpGV). The virus was first isolated in Mexico and subsequently studied and evaluated in Europe and North America. A variety of research including pathology, pathogenesis and histo- pathology of the virus, determination of virulence, development of production methods, field use, factors that influence efficacy, commercial development, formulation, and CM resistance to the virus has been conducted. Commercial products of CpGV are now produced in Europe and North America and used by orchardists worldwide. In this paper we present a comprehensive review of the CpGV literature and the role of the virus in integrated pest management. Keywords: codling moth; Cydia pomonella; granulovirus; resistance; pathology; commercial development; integrated pest management
Introduction Codling moth (CM), Cydia pomonella (L), (Lepidoptera: Tortricidae) is a serious pest of pome fruit (apple pear, crab apple, quince) and walnuts and can also survive in alternative Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 hosts, such as hawthorn (Crataegus spp.). CM is regarded as the most injurious insect pest of apple in most countries where apple is grown (Barnes 1991). It is usually controlled in conventional orchards with broad-spectrum insecticides such as azinphos-methyl † (Guthion ). Extensive use of broad spectrum pesticides has resulted in a variety of problems including negative environmental effects, insecticide resistance, outbreaks of secondary pests due to disruption of natural controls, and safety of pesticide applicators and the food supply. These concerns have increased the interest in and development of alternative means of control that have lower or no impact on beneficial organisms and
*Corresponding author. Email: [email protected] First published online 13 August 2008 ISSN 0958-3157 print/ISSN 1360-0478 online This material is declared a work of the United States Goverment and is not subject to copyright protection: approved for public release; distribution is unlimited. DOI: 10.1080/09583150802267046 http://www.informaworld.com 640 L.A. Lacey et al.
sensitive ecosystems (Lacey and Shapiro-Ilan 2008). An effective alternative to non- selective chemical insecticides with no impact on beneficial organisms is the CM granulovirus (CpGV). In this review, we will provide comprehensive background on the virus and its potential for incorporation into integrated pest management (IPM) in orchard agroecosystems.
Description, pathogenesis, histopathology and transmission of CpGV CpGV was originally isolated from infected CM larvae collected near Valle de Allende, Chihuahua, Mexico and described by Tanada (1964). CpGV is the type species for the genus Granulovirus within the family Baculoviridae (Theilmann et al. 2005; Jehle et al. 2006), and as such has a circular, double-stranded DNA genome and has both budded and occluded virus phenotypes (Crook, Spencer, Payne, and Leisy 1985; Crook 1986; Tanada and Hess 1991; Federici 1997). Granuloviruses are so named because of their granular appearance under high magnification in light microscopy. The granules, also referred to as occlusion bodies (OBs), consist of a viral encoded protein (granulin) matrix in which a single rod-shaped, enveloped virion is occluded (Federici 1986; Tanada and Hess 1991). The nucleocapsid consists of a protein coat containing the viral DNA genome (Figure 1). CpGV OBs are ovocylindrical and approximately 360 190 nm wide (based on measure of micrographs in Tanada 1964). Electron microscopy studies of the fine structure of the virus have also been reported by Stairs, Parrish, Briggs, and Allietta (1966), Tanada and Leutenegger (1968), and Hess and Falcon (1987) and its structure is typical of other granuloviruses (Federici 1986). CpGV is one of the most virulent granuloviruses, categorised as a type 2 granulovirus which is faster acting than types 1 or 3, with a broader range of tissues infected and resulting rupture of the integument. (Tanada and Hess 1991; Federici 1997). The OBs must Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008
Figure 1. Electron micrographs of the nucleocapsid and occlusion bodies (OBs) of the codling moth granulovirus. (A) shows a longitudinal section of the nucleocapsid. The (a) end of nucleocapsid orients toward the plasma membrane during the budding process while the (P) end is blunt and striated. The core (C) contains DNA and protein. (B) shows two OBs in cross-section. (N) is the capsid and core (Z) is an amorphous zone and membrane (M). The majority of the OB is a matrix of granulin. (L) indicates the outer envelop. Both bars are equal to 100 nm. Micrographs are from Tanada and Hess (1991). Copyright 1991. Reprinted with permission by CRC Press. Biocontrol Science and Technology 641
be consumed by larvae in order to produce infections. When neonate larvae ingest a lethal concentration of the virus, death ensues in as few as 3 days (Glen and Clark 1985; Brain and Glen 1989; Ballard, Ellis, and Payne 2000b; Lacey, Vail, and Hoffmann 2002). The LD50 has been estimated as low as 1.2 5 OBs per neonate larva (Sheppard and Stairs 1977; Harvey and Volkman 1983; Huber 1986) with higher estimates for number of OBs/mm2 of artificial diet (Laing and Jaques 1980; Huber 1981; Eastwell, Cossentine, and Bernardy 1999; Lacey et al. 2002). Older instars require higher doses of the virus (Keller 1973; Sheppard and Stairs 1977; Camponovo and Benz 1984). When older CM larvae are fed low dosages of the virus, they have a higher and longer rate of weight increase than uninfected larvae (Jans and Benz 1985). Following ingestion, the proteinaceous coat or granulin is dissolved in the alkaline pH of the midgut liberating the nucleocapsids. The nucleocapsids pass through the peritrophic membrane and then fuse with the microvilli of the midgut epithelium. After entering the cells, the nucleocapsids are transported to the nuclear membrane where the viral DNA genome appears to enter the nucleus by way of the nuclear pore. Virus replication or virogenesis takes place first in virogenic stroma in the nuclei of midgut cells and eventually in both the nuclei and cytoplasm when the nuclear membrane ruptures. Infection of these cells is transient without production of OBs (Hess and Falcon 1987; Federici 1997). Nucleocapsids are subsequently budded through the basal lamina membrane of the cells into the hemocoel (Hess and Falcon 1987). Infective virus may reach and infect other tissues via the hemolymph or through the tracheal junctions with these tissues (Federici 1997). A wide range of host tissues are infected, including, the fat body, tracheal matrix cells, hypodermis, and malpighian tubules (Tanada and Leutenegger 1968). These authors suggested that infection in the malpighian tubules could result in excretion of virus by this organ. Virus replication is followed by budding of nucleocapsids from infected cells to infect other cells or by occlusion of the nucleocapsids in granulin to form the characteristic OBs (Hess and Falcon 1987; Tanada and Hess 1991). Fat body cells produce the highest numbers of OBs. Figure 2 shows fully formed OBs in tracheal matrix cells. The OBs are infectious upon ingestion by other larvae. The length of time for CpGV development was shown by Sheppard and Stairs (1977) to be inversely proportional to virus dosage. The LT50 values for neonate larvae in their study ranged from 9.7 days for 3 OBs per larva to 3.7 days for 280 OBs per larva. Fifth-instar larvae responded similarly but to higher doses of virus. There are no obvious symptoms of the disease in older larvae until day 4 when they begin to swell and become glossy and moribund. Larvae stop feeding around day 7 as they begin to die. In the terminal phase of
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 the disease, they become milky and liquefy (Figure 3). Symptoms in younger larvae are similar but more difficult to detect and death ensues more quickly. Hess and Falcon (1987) provided a detailed electron microscope study of the sequence of development of CpGV within infected CM larvae. The life cycle of CM permits only limited natural exposure of larvae to occluded virus from contact with infected individuals or persistent virus left behind by them. The incidence of patent natural infections in nature is quite low or at least not routinely observed. The finding of small numbers of naturally infected larvae by several researchers in widely separate geographic locations indicates that vertical or horizontal transmission is necessary for maintenance of the virus in nature. Steineke and Jehle (2004) demonstrated horizontal transmission on fruit, but concluded that virus from infected individuals impacted subsequent infections only to a small degree. Etzel and Falcon (1976) demonstrated transmission of the virus between instars and stages in the laboratory. 642 L.A. Lacey et al.
Figure 2. Electron micrograph of infected tracheal matrix cells showing fully formed codling moth granulovirus occlusion bodies. Micrograph courtesy of Brian Federici. Copyright 1986. Reprinted with permission by CRC Press.
Light infections in older larvae permitted pupation (Falcon, Kane, and Bethel 1968; Biache, Severini, Guillon, and Quenin 1998b) and in some cases, emergence of adults (Etzel and Falcon 1976; Biache et al. 1998b). Females that survived light infections were capable of transmitting virus to eggs, but transovarial transmission was not shown. No Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008
Figure 3. Codling moth larvae patently infected with granulovirus. Photograph courtesy of Robert Jaques. Biocontrol Science and Technology 643
occluded virus was detected within eggs obtained from infected females using a fluorescent antibody technique (Etzel and Falcon 1976). However, Cossentine, Jensen, and Eastwell (2005) suggested the possibility of transovarial transmission in a CM mass rearing facility due to persistence of low level infections within the colony. When pre-neonate larvae were extracted from eggs prior to emergence and tested for the presence of virus using a polymerase chain reaction (PCR) assay, up to 40% carried detectable virus. It is possible that non-occluded viral DNA is passed within CM populations in this manner. Using PCR and an enzyme-linked immunosorbent assay (ELISA) assay, Eastwell et al. (1999) observed 23% of larvae collected from wild CM populations were positive for CpGV. The demonstration that a higher percentage of individuals carry viral DNA than the percentage of larvae with patent infections supports the possibility of transovarial transmission and or dormant infections. In addition to the surface of treated fruit, neonate larvae acquire virus from the surface of contaminated eggs and leaf surfaces. Ballard et al. (2000b) reported that CM larvae could acquire virus by walking over or browsing the surfaces of treated leaves in as few as 3.5 min. Ostensibly, larvae ingested the virus when browsing leaf surfaces or by contaminating the point of entry into the apple.
Selectivity and safety The specificity of CpGV for CM and safety to nontarget organisms has been documented by several researchers as reviewed by Gro¨ner (1986, 1990). Its use in orchard agroecosys- tems can contribute significantly to the conservation of other natural enemies (Dickler 1978; Glen, Wiltshire, Milsom, and Brain 1984; Riddick and Mills 1995; Suckling, Walker, and Wearing 1999; Arthurs, Lacey, and Miliczky 2007b; Simon, Defrance, and Sauphanor 2007). Although CpGV can infect other Cydia spp. and species in close genera in the family Tortricidae, the dosage required to kill these insects is significantly higher than that observed in CM. Falcon et al. (1968) reported unpublished data on the susceptibility of the Oriental fruit moth (OFM) Grapholita molesta (Busck) to CpGV. Quantitative bioassays of the Cyd-X formulation of CpGV by Lacey, Arthurs, and Headrick (2005a) revealed a 557- and 589-fold lower susceptibility of neonate OFM larvae compared with the LC50 and LC95 values derived for CM. Conceivably, label rates of CpGV used for CM control could potentially reduce OFM populations if significant feeding of early instars occurred. Pea moth (PM), Cydia nigricana (F.), is also infected by CpGV, but is more than 12-fold less susceptible than CM (Payne 1981). Geissler (1994) reported 71.9% mortality of PM in field
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 trials of the Granupom formulation of CpGV. Preliminary laboratory and field studies of the Madex formulation against the pine shoot moth, Rhyacionia buoliana (Denis and Schiffermu¨ller), were reported by Skrzecz (2000). Extremely high rates of the virus (3 1012 OB/mL) killed up to 71% of larvae. However, notable reduction of feeding by R. buoliana larvae was observed in field trials of the virus. Reiser, Gro¨ner, and Sander (1993) reported on the susceptibility of false codling moth (FCM), Cryptophlebia leucotreta Meyrick, to CpGV and proposed it as an alternate host for virus production. Both CM and FCM produced the same amount of OBs per larva but 104 times the inoculum was required to infect FCM fifth instars than the amount required to infect CM. The authors contended that the ease of rearing FCM compensated for the greater amount of inoculum. Eastwell et al. (1999) demonstrated susceptibility in two tortricid leafrollers (Archips argyrospila (Walker) and Choristoneura rosaceana (Harris)) to very high concentrations of virus (9.1 104 and 106 OBs per mL, respectively). Glen et al. (1984) reported no effect of CpGVon two 644 L.A. Lacey et al.
other lepidopteran orchard pests, Archips podanus (Scopoli) (Tortricidae) and Blastodacna atra (Haworth) (Agonoxenidae). Research cited by Gro¨ner (1986, 1990) demonstrated that CpGV was not infectious for a wide variety of other insects including silkworms and honeybees (Gro¨ner, Huber, Krieg, and Pinsdorf 1978; Gro¨ner 1986, 1990). In field trials of CpGV (6.6 1012 OB/ha) and spinosad (EntrustTM) (210 g/ha) for control of CM, populations of non-target organisms were not affected by CpGV, but some were adversely affected by application of spinosad (Arthurs et al. 2007b). Arthurs and Lacey (2004) recovered the CM larval parasitoid Mastrus ridibundus Gravenhorst (Hymenoptera: Ichneumonidae) in orchards treated with CpGV. Baculoviruses, particularly the NPVs, have been extensively tested for their safety to nontarget organisms including vertebrates (Saik, Lacey, and Lacey 1990). Safety testing of granuloviruses on vertebrates has been considerably less extensive but the specificity of CpGV has been confirmed in a study by Do¨ller and Huber (1983). They concluded that CpGV was not infectious for rabbits and mice.
Bioassay and production of virus Several authors have described methods for the bioassay of CpGV preparations and products (Keller 1973; Sheppard and Stairs 1977; Laing and Jaques 1980; Huber 1981; Glen and Payne 1984; Lacey et al. 2002). Most quantitative bioassays are conducted on artificial medium with neonate larvae. The surface is treated with CpGV suspensions of various concentrations and allowed to dry before adding larvae. Bioassays conducted with one larva per vial eliminates antagonistic interactions between larvae. Typically, for probit analysis and determination of LC50 and LC95, five to seven concentrations of virus are used such that mortalities between 10 and 90% are produced with at least two concentrations below and two above the LC50. Bioassays of older larvae have also been conducted using higher concentrations of virus to achieve the appropriate range of mortalities. The numbers of larvae used per concentration per date varies among researchers. Replicate tests are usually run on three or more separate dates. Bioassays using one or more discriminating dosages have also been used to determine product quality and stability, resistance in CM populations, and as initial tests to determine activity against other potentially susceptible species. Laboratory assays have also been conducted with virus-treated leaf disks and fruit (Glen and Payne 1984; Glen and Clark 1985; Ballard et al. 2000b; Arthurs, Lacey, and Fritts 2005; Lacey and Arthurs 2005). A technique that permits even virus coverage of fruit and exposure to simulated solar radiation was developed by
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Lacey and Arthurs (2005). Production of the amounts of CpGV that are necessary for field trials and commercial products requires the use of older larvae (Keller 1973; Brassel 1978; Huber 1981; Glen and Payne 1984). Huber (1981) developed two methods for the production of CpGV in CM, one for purified virus used in basic research and one for the production of unpurified material for field trials. For the latter, larvae that are infected and killed by the virus infection are processed together with their diet. Brassel (1978) dipped later fourth-instar or early fifth-instar larvae into a suspension containing 104 virus particles/mL resulting in a high rate of infection and maximum larval weight. Infection was more efficient in diapause destined larvae (Brassel 1978). In vitro replication of CpGV was first achieved by Naser, Miltenburger, Harvey, Huber, and Huger (1984) and Naser (1986) in CM cell lines, however virus production was low. Further efforts and improved virus production and cell line stability were reported by Biocontrol Science and Technology 645
Winstanley and Crook (1993). Additional advances with this method will be needed to develop efficient and cost effective invitro mass production of the virus on a commercial scale.
Field applications Evaluation of experimentally and commercially produced virus has been reported by several authors. Successful trials were conducted across Europe, North America, Argentina, New Zealand, Australia and South Africa (Table 1). The level of population control depends on the dosage, frequency and timing of virus application, CM population pressure, the number of generations and environmental conditions. Dosages in the order of 4.6 1012 to 1013 OB/ha provided effective control. Timing of virus application is critical for control of the first CM generation beginning at first egg hatch (111 1398C degree days (200 2508F degree days)) and continuing until hatch is complete. Lower dosages of virus have also been used. Kienzle, Gernoth, Zebitz, and Huber (2003a) reported good CM control using low concentrations of the virus in conjunction with synthetic insecticides and lure and kill methods using CM pheromone. Dickler and Huber (1986) reported nine applications of one-tenth of the regular dosage of CpGV resulted in CM control that was comparable to fewer applications of the full dosage. Similar results were observed by Helsen, Blommers, and Vaal (1992) after four applications of the full rate (0.5 L/ha) and 10 weekly applications of one-tenth the full rate. Sheppard and Stairs (1976) reported reductions of infestations in apples ranging from 0 to 42% after applications of 107 OBs (0.002 larval equivalents, L.E.) per tree to 109 OBs (0.2 L.E.) per tree. They observed 15 30% of larvae infected with CpGV in apples from untreated trees and concluded that the virus increased and spread within the orchard. The authors speculated that the spread of virus could be attributed to spray drift or to epizootics in treated larvae which spread to unsprayed trees. The specific mechanism for dissemination was not demonstrated. It is also possible that females surviving virus treatment could transmit CpGV to their eggs (Etzel and Falcon 1976). Treatment intervals depend on the same variables that determine effective population control (number of CM generations per year, population pressure, persistence of effective levels of virus, and environmental conditions). In order to accomplish effective CM control, CpGV must be reapplied throughout the peak egg hatch period. The recommended application intervals for multivoltine populations range from 7 to 14 days (Keller 1973; Huber and Dickler 1977; Dickler and Huber 1986; Jaques 1990; Stara´ and Kocourek 2003; Arthurs and Lacey 2004; Arthurs et al. 2005). The number of applications
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 will vary depending on the number of generations. For example, in Nova Scotia where there is only one CM generation per year, Jaques, Hardman, Laing, and Smith (1994) reported that only one to two applications of CpGV were usually needed. Measurement of the efficacy of season long viral applications is usually determined by assessing fruit damage, especially deep entries of larvae and by sampling the number of over wintering larvae in tree bands (Huber and Dickler 1977; Glen and Payne 1984; Lacey, Arthurs, Knight, and Huber 2007). Two of the principle complaints about CpGV by growers are shallow entries of neonates into fruit and the need for frequent reapplication. Despite the relatively rapid speed of kill, exposed larvae live long enough to damage fruit. Because larvae must ingest the virus, contact with the fruit and shallow entries (stings) are inevitable (Glen and Clark 1985). However, as populations are effectively reduced, entries into fruit are usually reduced to acceptable levels (Pasquier and Charmillot 1998). Since most infected larvae die 646 L.A. Lacey et al.
Table 1. Field application of codling moth granulovirus for control of codling moth, Cydia pomonella.
North America Falcon et al. (1968) Apple Jaques et al. (1977, 1981) Apple Falcon and Berlowitz (1986) Apple Jaques et al. (1987, 1994) Apple Jaques (1990) Apple Falcon and Huber1 (1991) Apple Vail et al. (1991) Walnut Riddick and Mills (1995) Apple Cossentine and Jensen (2004) Apple Arthurs and Lacey (2004) Apple Lacey et al. (2004) Apple Arthurs et al. (2005, 2006) Apple Arthurs et al. (2007b) Pear Rashid et al. (2001) Apple Lacey et al. (2007)1 Apple, pear Argentina L. Cichon (pers. comm.) Apple Australia Falcon and Huber1 (1991) Apple New Zealand Wearing (1993) Apple Suckling et al. (1999) Apple South Africa Falcon and Huber1 (1991) Apple Europe Keller (1973) Apple Huber and Dickler (1975, 1977) Apple Dickler (1978) Apple Glen and Payne (1984) Apple Dickler and Huber (1986) Apple Charmillot et al. (1984, 1998) Apple Burgerjon (1986) Apple Blommers et al. (1987) Apple, pear Falcon and Huber1 (1991) Apple Audemard et al. (1992) Apple Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Helsen et al. (1992) Apple Guillon and Biache (1995) Apple Trematerra et al. (1997) Apple Biache et al. (1998a) Apple, pear Cross et al. (1999)1 Apple, pear Kienzle et al. (2003a) Apple Stara´ and Kocourek (2003) Apple Simon et al. (2007) Apple Israel Falcon and Huber1 (1991) Apple USSR (Kazak) Falcon and Huber1 (1991) Apple
1General reviews that include several references regarding field use of CpGV. Biocontrol Science and Technology 647
just below the surface of the fruit (Falcon et al. 1968; Glen and Clark 1985), some growers are able to market stung fruit (Jaques 1990; Lacey et al. 2007). Frequent reapplications are required not only in response to population pressure but also due to solar inactivation of the virus (see also formulation for UV protection). The amount of time the virus persists (and remains virulent) varies according to spray coverage and dosage and field conditions (amount of solar radiation (conversely number of days with cloud cover), temperature, and precipitation including irrigation). Exposure to solar radiation (UVB, 280 320 nm) is the most critical factor limiting the persistence of entomopathogenic viruses (Krieg, Gro¨ner, Huber, and Zimmermann 1981; Jaques 1985; Ignoffo 1992). Krieg et al. (1981) and Lacey and Arthurs (2005) described the sensitivity of CpGV to short wave UV. Shading and microhabitats on the host plant and in the environment can protect some viruses from solar degradation and enable long-term persistence (Cory and Evans 2008). A measurement of field stability of virus includes the collection of sprayed fruit or leaves at various intervals after application and challenge in the laboratory with neonate larvae. Glen and Payne (1984) described a technique to measure inactivation of CpGV that involved washing it from leaves of sprayed trees at various intervals post-treatment, and incorporating the rinse into artificial diet for bioassay. They showed that, although CpGV infectivity was reduced by half in 3 days, some activity persisted as long as 4 8 weeks after spraying. Arthurs and Lacey (2004) reported early season applications of label rates of 3 CpGV products remained highly effective for the first 24 h (producing 94% larval mortality) and moderately effective after 72 h (71% mortality) declining to 50% of its original value after 8 days (early summer) during dry sunny conditions. Significant activity remained for up to 14 days, suggesting prolonged survival of the virus in UV-protected locations, such as the calyx of fruit. The decline to 50% activity was more rapid (4 days) in mid-summer, but temperature above 358C could also have a played a role. Cossentine and Jensen (2004) observed the highest mortality of larvae fed on apple or leaves that were sprayed with the Virosoft formulation and collected 1 day later. Significant, but lower larval mortality was also recorded on apples collected 5 and 8 days post-treatment. Lacey, Arthurs, Knight, Becker, and Headrick (2004) reported a steady decline in activity of CpGV (Carpovirusine) on field-collected sprayed fruit 1 3 days post-treatment despite the addition of adjuvants. Other studies have estimated half-lives of CpGV of 2 3 days (Huber 1980; Jaques, Laing, Laing, and Yu 1987; Jaques 1990; Charmillot, Pasquier, and Scalo 1998; Pasquier and Charmillot 1998; Kienzle, Schulz, Zebitz, and Huber 2003c) and up to 10 20 days (Stara´ and Kocourek 2003). Rezapanah, Assady, Esmaili, and Ghanbalani (1996) reported a half Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 life as short as 4 h using a leaf disk assay of field applied virus. This is markedly shorter than the studies reported above. Their results could due to the bioassay method employed. What could have been construed as less virus activity could have been due to reduced feeding.
Commercial development CpGV was first mass cultured and field tested in California from 1965 to 1972 (Falcon et al. 1968; Falcon and Berlowitz 1986). It is the most effective microbial control agent yet available for control of CM. Sandoz Corporation produced the first commercial formulation (SAN 406) and was granted an experimental use permit by the EPA in 1981. SAN 406 was successfully tested worldwide between 1981 and 1984. Despite successful results, Sandoz terminated all work on insect viruses in 1984 and the commercial development of CpGV products in the USA was largely terminated until recently. 648 L.A. Lacey et al.
In Europe, the first field tests on CpGV were conducted in 1970. In 1979, the Commission of European Communities (CEC) initiated the ‘Biological Control in Apple Orchards’ program (Falcon and Huber 1991). The CEC supported research on the use of CpGV in orchards throughout Europe. After Sandoz terminated work on SAN 406, European government agencies and scientists and a Swiss scientist working in conjunction with companies, developed and commercialized CpGV products. This collaborative effort led to the registration of 3 products including MadexTM registered in 1988 by Andermatt Biocontrol, Switzerland, GranupomTM registered in 1991 by Hoerst, Germany and CarpovirusineTM registered in 1993 by Calliope, France. CpGV is estimated to be used on 100,000 ha in Europe annually (Eberle and Jehle 2006). Currently there are three formulations registered in the USA. They include Cyd-XTM registered in 1995 by Certis USA, VirosoftTM registered in 2000 by Biotepp, and Carpovirusine registered in 2001 by Sumitomo, now marketed by Arvesta Corporation. Concentrations of virus in commercial products range from 1013 to 3.4 1013 OBs per liter. The only product that is currently registered in Canada is Virosoft. CpGV is extensively used in organic pome fruit systems and increasingly in conventional systems. It is estimated that CpGV is now used on 8100 12,200 ha in North America annually (D. Thomson, personal communication). All commercial products before 2000 were based on the Mexican isolate of CpGV (CpGV-M). The Virosoft CP4 product is based on virus isolated in the CP4 region of Quebec, Canada (Vincent, Andermatt, and Vale´ro 2007). Other isolates of CpGV have been discovered in England, Russia and Iran (Crook et al. 1985; Rezapanah, Kharrazi- Pakdel, Kamali, and Huber 2002).
Formulation Like other entomopathogens, formulation of CpGV in suitable carrier(s) is required to maximise storage potential and application and effectiveness in the field (Jones and Burges 1998). Currently all CpGV products are manufactured and sold as suspension concen- trates, although freeze-dried wettable powder formulations are currently being developed (D. Thomson, personal communication). Effective formulations may also include the use of various additives either in the product or mixed into spray suspensions at the time of application.
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Product storage potential The two principle concerns of commercial producers are consistent product potency and stability (Richards 1986). A shelf life of 18 months has been recommended to allow microbial pesticides to be distributed, stored and used without undue loss in effectiveness (Couch and Ignoffo 1981). Products usually include adjuvants that stabilise the virus and enable ease of suspension in water. How formulations are stored can have a significant effect on retention of larvicidal activity. Some producers ship frozen product and advise retailers and growers to keep the virus frozen until use. Brassel (1978) reported that CpGV could best be stored when glycerin was added and the preparation kept at 208C. Geissler (1994) stored the Granupom formulation of CpGV at 188C for 3 years and concluded that its activity for PM (C. nigricana) was similar to a recently produced batch of the virus. Lacey, Headrick, and Arthurs (2008) observed no decline in larvicidal activity from Cyd-X and Virosoft formulations of CpGV stored at 28C for 3 years or room temperature for over 2 years. Biocontrol Science and Technology 649
However, exposure of CpGV formulations to 358C significantly reduced survival of the virus in 20 40 weeks (Lacey et al. 2008). On the other hand, Fritsch and Huber (1985) demonstrated that exposure of CpGV to temperatures of up to 758C for 160 min caused no significant loss of activity. The precise mechanism(s) responsible for decline of CpGV activity following storage at higher temperatures could be due to denaturing of viral DNA and or the protein coat.
Spreaders/stickers Various wetting and sticking surfactants are generally recommended (or included in some CpGV products) to improve mixing, reduce surface tension and increase deposition over plant surfaces. Commercially available wetting agents include Tritons, Tweens and organosilicones, while stickers, including vegetable gums, gluten, celluloses, or terpene polymers are routinely used to reduce ‘wash off’ through rainfall and irrigation (Burges and Jones 1998).
UV screens Given the short half lives of CpGV under field conditions, formulation to protect CpGV from UV degradation, particularly the damaging UV portion 280 320 nm, has been investigated by several researchers. Suncreens protect OBs either by reflecting harmful rays or by selective absorption, converting shorter wavelengths to harmless longer ones (Burges and Jones 1998). The reflectors titanium dioxide (Bull, Ridgway, House, and Pryor 1976; Farrar, Shapiro, and Javaid 2003) and iron oxide (Asano 2005) have increased the activity of the nucleopolyhedrovirus (NPV) of Heliocoverpa spp. and granulovirus of the oriental tea tortrix Homona magnanima Diaknoff, respectively, although we find no reports of similar reflectors tested with CpGV. A number of materials which absorb specific wavelengths, including specialised dyes and chemicals such as Congo Red and stilbene derivatives, and other more natural, readily available and cheaper materials that adsorb over a greater range have been tested to improve the residual activity of microbial pesticides for various other Lepidoptera (reviewed by Burges and Jones 1998). There are few comparable studies with CpGV, although molasses, sucrose and skimmed milk powder have been reported to slightly improve persistence or uptake (acting as a phagostimulant) of CpGV. The rates typically used for these additives, e.g.]1% (w/v), are likely to be too Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 high for routine field use (Keller 1973; Glen and Clark 1985; Charmillot et al. 1998; Ballard, Ellis, and Payne 2000a). More recently, a method to encapsulate viral OBs in lignin via spray drying has been developed and tested with CpGV (Arthurs, Lacey, and Behle 2006). Laboratory tests with irradiated fruit showed that up to 95% CM mortality was achieved with the lignin formulation compared with 56 67% for a commercial CpGV product, although further improvements are required to achieve the same results in field situations. Several proprietary ‘particle film’ materials, recently marketed as sunburn protectants for fruit, may provide similar protection for CpGV. Although one wax-based product did not improve residual activity (Lacey et al. 2004), research into the use of several other materials, such as kaolin clay, is currently underway. Lacey and Arthurs (2005) describe a laboratory technique using a solar simulator and sectioned apples to test putative UV protective compounds for CpGV. 650 L.A. Lacey et al.
Feeding stimulants and larval attractants The limited feeding of CM prior to fruit penetration is a key biological factor that constrains the effectiveness of CpGV. Conceptually, adjuvants that increase larval exposure and ingestion of residues should improve its effectiveness. Various plant extracts and similar materials have been tested as phagostimulants with microbial pesticides. Various products are commercially available for this purpose, although mainly for use with Bacillus thuringiensis Berliner (Burges and Jones 1998). Molasses is reported as one of the most effective feeding stimulants for lepidopteran larvae. Ballard et al. (2000a) reported 15% cane molasses reduced the medium exposure time required for CM neonates to acquire a lethal dose of CpGV (e.g. from 269 to 5 min) although the authors noted a more realistic concentration of 1% (v/v) was not effective. Other potential CM phagostimulants include monosodium glutamate (Pszczolkowski, Matos, Zahand, and Brown 2002) and trans-1-aminocyclobutane-1,3-dicarboxylic acid (trans-ACBD) (Pszczolkowski and Brown 2004). In spite of promising work on phagostimulants, successful field trials demonstrating improved performance with CpGV at economic rates are lacking. The use of kairomones to enhance control of CpGV has received recent attention. Pear ester is an attractant for both adult and neonate CM. By increasing the distance eggs are laid from fruit (Pasqualini et al. 2005) and masking host odors, pear ester may increase neonate wandering on foliage thus increasing feeding of treated leaf surfaces (Ballard et al. 2000b). Light (2007) tested a microencapsulated formulation of pear ester (PE-MEC) and was able to further reduce injury in walnut by 47% with an 8-spray seasonal program of CpGV plus PE-MEC compared with CpGV alone. However, Arthurs, Hilton, Knight, and Lacey (2007a) reported inconsistent results in similar tests on apple and pear, and suggested that practical improvements in formulation and application strategies (e.g. to optimise and maintain attractive release rates) were needed.
Molecular studies and genetic enhancement Much of the earlier molecular studies on CpGV were accomplished by Norman Crook and associates and set the stage for continuing developments. Characterisation and comparison of seven CpGV isolates from Europe, North America and New Zealand using restriction enzyme analysis showed only small genotypic differences among the isolates (Crook et al. 1985). Interestingly, the isolates from Russia and England showed greater differences between them than either did when compared to the CpGV-M strain. Harvey and
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Volkman (1983) compared three different sources of CpGV using biological and biochemical techniques. Restriction enzyme analysis was conducted on the CpGV-M strain maintained separately for 9 years at two laboratories (Berkeley, CA, USA and Darmstadt, Germany). The two cultures were 99.94% homologous and no differences were found in molecular weights of enveloped virion polypeptides. However, they report some biochemical differences between the CpGV-M isolate and an isolate from Russia. In bioassays, the virulence of the two cultures of the CpGV-M isolate was similar, but the Russian isolate was less virulent. Eastwell et al. (1999) developed a CpGV-specific ELISA and PCR primers to detect the virus in a laboratory colony and wild populations of CM. They determined that the strain found in their colony (maintained in Summerland, British Columbia, Canada) was identical to the CpGV-M isolate. PCR assays have also been developed by Biache, Perchat, Quenin, and Aupinel (1999) and Kundu, Stara’, Kocourek, and Pultar (2003) for detection of CpGV DNA in CM populations. Biocontrol Science and Technology 651
Crook et al. (1985) began research on the physical mapping of the CpGV genome that revealed the location of the granulin gene. Subsequent research by Crook, James, Smith, and Winstanley (1997) led to a comprehensive physical map of the CpGV genome and sequence analysis of the gene responsible for granulin production. Luque, Finch, Crook, O’Reilly, and Winstanley (2001) reported on the complete sequencing of the CpGV genome and the genetic similarities with granuloviruses of two other lepidopterans (Xestia c-nigrum [L.] (Noctuidae) and Plutella xylostella [L.] (Plutellidae)). Hilton and Winstanley (2007) systematically scanned the entire genome of CpGV for origins of DNA replication using an infection-dependent DNA replication assay in the granulovirus-permissive CM cell line (Cp14R). They concluded that the previously proposed non-homologous region origin of replication did not replicate in their assay. Research conducted by Jehle and associates further elucidates the genetics of CpGV. Several studies of the transposons of CpGV are presented by Jehle and co-workers (Jehle, Fritsch, Nickel, Huber, and Backhaus 1995; Jehle, van der Linden, Backhaus, and Vlak 1997; Jehle, Nickel, Vlak, and Backhaus 1998) and Arends and Jehle (2002). Kang, Crook, Winstanley, and O’Reilly (1997) conducted research that provided the complete sequence and transposon mutagenesis of the BamHI J fragment of CpGV. Kang, Tristem, Maeda, Crook, and O’Reilly (1998) also identified and characterised CpGV cathepsin and chitinase genes. Selection of CpGV strains not involving molecular methods has also been presented. The promoter regions of the granulin gene are of particular interest because of the high levels of expression of granulin protein. This information expanded the potential for genetic improvement. Crook and Winstanley (1990) presented some of the possibilities for genetic engineering including the insertion of toxin genes such as those found in B. thuringiensis. Development of a strain of CpGV lacking the egt gene was reported by Winstanley, Jarrete, and Morgan (1998). Larvae infected by the modified virus are unable to produce the ecdysteroid-UDP glucosyl transferase, the enzyme responsible for regulating the molting hormone ecdysone. Studies by Winstanely et al. (1998) indicate that the egt strain kills more rapidly and reduces feeding in first-instar larvae thereby reducing shallow entry damage. Before genetically modified CpGV or any other Baculovirus is released, a thorough understanding of the potential consequences of the virus in the environment is needed. Fritsch, Huber, and Backhaus (1990) outlined studies to use CpGV as a tool in the risk assessment of genetically engineered baculoviruses. The goal of their study was to examine and quantify the possibility of genetic exchange between different viruses co-infecting the
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 same tortricid host. Co-infection of C. leucotreta with CpGV and the C. leucotreta granulovirus (CrleGV) was proposed. Subsequently, Jehle, Fritsch, Huber, and Backhaus (2003) observed intra and inter-specific recombination of Crle and CpGV during co- infection of C. leucotreta larvae.
CpGV resistance The ability of CM to develop resistance to a variety of chemical pesticides has been reported in Europe and North America (Sauphanor, Bouvier, and Brosse 1998, Dunley and Welter 2000; Boivin, Chabert d’Hieres, Bouvier, Beslay, and Sauphanor 2001; Boivin, Bouvier, Chadoeuf, Beslay, and Sauphanor 2003; Reyes et al. 2007). CpGV has been proposed as a tool to manage CM resistance to chemical pesticides (Charmillot and Pasquier 2002b; Kienzle, Schulz, Zebitz, and Huber 2003b). However, CM resistance to 652 L.A. Lacey et al.
CpGV has recently been reported in Germany and France in organic orchards treated with multiple applications of CpGV over an extended period (Fritsch, Undorf-Spahn, Kienzle, Zebitz, and Huber 2005; Eberle and Jehle 2006; Sauphanor, Berling, Toubon, Reyes, and Delnatte 2006). Resistance to CpGV has now been found in Switzerland and Italy (J. Jehle, personal communication). Resistance ratios in some CM populations exceed 1000 (Asser- Kaiser et al. 2007). Laboratory studies reveal that rapid development of extreme resistance (100,000 resistance ratio) is possible due to sex-linked inheritance of a dominant-resistant gene (Asser-Kaiser et al. 2007). Interestingly, Biache et al. (1998b) attempted to generate resistance in a laboratory population of CM. After nine generations, larvae were still susceptible to the virus. Studies by German scientists are underway to identify molecular markers that can detect resistance in CM populations more quickly than bioassays using F1 larvae (J. Jehle, personal communication). Research by this group also includes the identification of the gene responsible for elevated levels of resistance to CpGV. A European project (SustainCpGV) seeks to identify and characterise more virulent CpGV isolates. Currently most CpGV products that are used for CM control are based on the CpGV-M isolate. At least four other related CpGV strains have been reported from broadly separated countries (England, Canada, Russia, and Iran) (Crook et al. 1985; Vincent et al. 2007; Zingg and Kessler 2008). Some of these differ genetically from CpGV-M (Crook et al. 1985; Vincent et al. 2007). The SustainCpGV group (www.sustaincpgv.eu) proposes to characterise these different CpGV isolates in order to understand how they can be best used in resistance management programs. The group also proposes to search for and characterise CpGV isolates from Central Asia (the putative center of origin of CM) that can serve as alternatives to the currently used CpGV-M strain and which may assist in the fight against the emerging virus resistance of CM. Also of interest, two of the three commercial producers in Europe have identified isolates of CpGV that overcome CM resistance (http:// www.sustaincpgv.eu). Zingg and Kessler (2008) reported that Madex , capable of overcoming resistance, was developed through laboratory selection of a strain of the original CpGV-M isolate that killed resistant larvae. An Iranian isolate (I12) of CpGV can also kill larvae that are resistant to the CpGV-M isolate (Eberle, Asser-Kaiser, Sayed, Nguyen, and Jehle 2008). Because CpGV-M is being increasingly used in North America, the potential for development of resistance should be a cause for concern (Warner 2007; Lacey 2008). An integrated approach that alternates other soft interventions with CpGV products should be
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 considered, especially when the virus is used extensively within a region. Determination of CpGV susceptibilities of CM in orchards with treatment success and those with suspected treatment failure in the Pacific Northwest region of North America should be undertaken. Baseline data of susceptible populations will provide the necessary foundation for determining future signs of resistance. Management strategies that will maintain the efficacy of CpGV are needed before a decline in CM susceptibility is detected. Various factors could influence the probability that resistance in CM to CpGV would develop in North America. In addition to the frequency of genes responsible for resistance in North American CM populations, the number of years that CpGV has been used against a given population, the number and frequency of applications per season, the size of virus treated populations and their proximity to CM that are not treated with CpGV, could help to determine if and when resistance will develop. Biocontrol Science and Technology 653
Role of CpGV in orchard IPM In Europe, CpGV is annually applied on approximately 100,000 ha of pome fruit. The virus is a key component in the management of CM insecticide resistance in France (Anon. 2007) and Switzerland (Charmillot and Pasquier 2002b). In Germany and France, CpGV is extensively deployed in conventional orchards in conjunction with insecticides and pheromone-mediated mating disruption as a long-term CM population management tool (Biache, Guillon, and Quenin 1998a; Kienzle et al. 2003c). In contrast, in North America, CpGV is predominantly used in organic orchards where it is deployed in conjunction with pheromone-mediated mating disruption technology and other soft methods for CM control. Additionally, in British Columbia, Canada, the virus has been used in conjunction with sterile insect release (SIR) (J. Cossentine, personal communication and http:// www.agf.gov.bc.ca/treefrt/product/03organic.pdf). Concerns of conventional orchardists regarding microbial control agents are that they require frequent application and are too selective thereby allowing other pests to survive. Although broad-spectrum chemical pesticides control CM and a wide range of other insect pests, they disrupt natural enemies and other beneficial insects. When harmful interventions are minimised or eliminated in apple and pear orchards, natural enemies and other nontarget populations increase and become more diverse (LeRoux 1961; Madsen and Madsen 1982; Audemard 1987; Blommers, Vaal, Freriks, and Helsen 1987; Prokopy, Mason, Christie, and Wright 1996; Gurr, Thwait, and Nicol 1999; Nicholas, Thwaite, and Spooner-Hart 1999; Suckling et al. 1999; Epstein, Zack, Brunner, Gut, and Brown 2000, 2001; Miliczky, Calkins, and Horton 2000; Simon et al. 2007). One of the key components of IPM in orchards and other crops is the controlling effects of natural enemies on pest insects and mites (DeBach 1964; van den Bosch, Messenger, and Gutierrez 1982). While effective in controlling CM, CpGV will not be a stand alone control method, especially when other insect pests exceed economic injury levels. For CM control, population suppression effects will be enhanced by combining the virus with other interventions. These include: pheromone-mediated mating disruption; alternation with other soft insecticides (e.g. horticultural mineral oil, spinosad, etc.); use of entomo- pathogenic nematodes (Steinernema spp. and Heterorhabditis spp.); other biological control agents (predators and parasitoids); and cultural control (use of banding around trees to capture and remove overwintering larvae and good orchard sanitation (i.e. removal of infested thinning apples and potential overwintering habitats)). For example, Trematerra, Borserio, and Tonesi (1996), Min˜arro and Dapena (2000) and Charmillot and Pasquier (2002a) reported on the effectiveness of mating disruption and CpGV for Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 enhanced CM control. Blommers et al. (1987) presented data on the control of CM and the summer tortrix, Adoxophyes orana (Fischer and Rosslertamm), with viruses and mating disruption and the role parasitoids and predators played in the control of A. orana and a variety of other orchard pests. Supplementing the control of neonate CM larvae with CpGV, entomopathogenic nematodes can be used to target overwintering larvae (Kaya, Joos, Falcon, and Berlowitz 1984; Lacey, Neven, Headrick, and Fritts 2005b; Lacey, Arthurs, Unruh, Headrick, and Fritts 2006). thereby reducing the numbers of emerging moths in the following growing season. Alternating CpGV treatments with spinosad was reported by Arthurs and Lacey (2004) as a strategy used by organic orchardists for control of CM as well as other pest insects. However, care must be taken with timing of spinosad applications in orchards and other agroecosystems due to its negative effects on certain natural enemies (Williams, Valle, and Vinuela 2003; Arthurs et al. 2007b). Bacillus thuringiensis is used to specifically target several other lepidopteran 654 L.A. Lacey et al.
orchard pests such as leafrollers, budmoths and fruitworms (Lacey et al. 2007; Lacey and Shapiro-Ilan 2008). Cossentine, Jensen, and Deglow (2003) demonstrated a strategy for use of B. thuringiensis to minimise its impact on parasitoids of the targeted leafroller, C. rosaceana. Because of their safety and selectivity, CpGV, B. thuringiensis, other biopesticides and naturally occurring entomopathogens are ideal components of IPM systems that allow predators and parasitoids to function. Although there are several reports on the innocuous nature of CpGV and B. thuringiensis toward beneficial insects and other nontarget organisms (Gro¨ner 1990; Lacey and Siegel 2000), there are few studies on the specific interactions between entomopathogens and arthropod natural enemies of CM (Lacey and Unruh 2005). Increased biological control will be favored when there is compatibility between parasitoids and pathogens (Brooks 1993; Begon, Sait, and Thompson 1999). Because CpGV targets neonate larvae, death of parasitoids that attack later instars would be minimised. For example, CpGV infects neonate CM larvae while the parasitoid M. ridibundus searches for and attacks cocooned fifth-instar larvae demonstrating complimentary activity of the two agents (Lacey and Unruh 2005). Similar positive interaction between CpGV and predators has also been reported. For example, the survival of mite predators of the European red mite, Panonychus ulmi (Koch), following CpGV applications kept the pest mite population below economic injury levels. This was not the case when chemical pesticides disrupted its natural enemies (Glen et al. 1984). On the other hand, CpGV resulted in the indirect decline of the parasitoid Ascogaster quadridentata Wesmael due to premature death of host CM larvae before the parasitoid could complete development (Falcon and Huber 1991). Effective control of CM could also deprive these and other CM-specific parasitoids of hosts. Other strategies to increase natural enemies of CM, leafrollers and other pest insects and mites in orchards include environmental manipulation such as ground cover management (Dickler 1978; Horton et al. 2003; Min˜arro and Dapena 2003; Brown and Tworkiski 2004; Mathews, Bottrell, and Brown 2004) and provision of plants that provide nectar and harborage for beneficial insects or harbor alternate hosts of natural enemies of tree fruit pests (Stephens, France, Wratten, and Frampton 1998; Fitzgerald and Solomon 2004; Irvin et al. 2006; Simon et al. 2007). Several other components of IPM in orchards are reviewed by Asquith, Croft, Hoyt, Glass, and Rice (1980), Huber et al. (1990), Prokopy, Cooley, Autio, and Coli (1994), Blommers (1994), MacHardy (2000) and Lacey and Shapiro-Ilan (2008).
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Microbial control agents are often compared with chemical pesticides on the basis of cost and spectrum of insecticidal activity alone. An analysis of the cost versus benefits of any control agent should also include their safety to applicators, the food supply, beneficial organisms and their lack of negative environmental effects. Microbial control agents provide effective, safe and environmentally friendly means of pest control (Lacey, Frutos, Kaya, and Vail 2001; Kaya and Lacey 2007). An example of one of the major benefits of using softer methods for insect control is presented in a recent study conducted by Lu, Barr, Pearson, and Waller (2008). They demonstrated the presence of organophosphate (OP) metabolites in the urine of children that consumed fruits and vegetables produced with chemical pesticides. Children that consumed only organically produced food (i.e. without use of conventional pesticides) showed no evidence of these metabolites. Their findings demonstrate that dietary intake of OP pesticides represents the major source of exposure in young children. CpGV and other soft means of pest control provide Biocontrol Science and Technology 655
alternatives to conventional chemical pesticides and play significant roles in sustainable agriculture, a healthier planet and safer food.
Acknowledgements We are grateful for the constructive reviews of the manuscript by Joan Cossentine, Don Hostetter and Wee Yee. The comments and suggestions of our anonymous reviewers are appreciated and improved the manuscript. We also thank our colleagues who have furnished literature, comments and suggestions for the manuscript.
References Anon. (2007), INRA Note Nationale: Carpocapsae des Pommes et Poires, Institut Nationale de la Recherche Agronomique, p. 3 Arends, H.M., and Jehle, J.A. (2002), ‘Homologous Recombination between the Inverted Terminal Repeats of Defective Transposon TCp3.2 Causes an Inversion in the Genome of Cydia pomonella Granulovirus’, Journal of General Virology, 83, 1573 1578. Arthurs, S.P., and Lacey, L.A. (2004), ‘Field Evaluation of Commercial Formulations of the Codling Moth Granulovirus (CpGV): Persistence of Activity and Success of Seasonal Applications against Natural Infestations in the Pacific Northwest’, Biological Control, 31, 388 397. Arthurs, S., Lacey, L.A., and Fritts, R. Jr. (2005), ‘Optimizing the Use of the Codling Moth Granulovirus: Effects of Application Rate and Spraying Frequency on Control of Codling Moth Larvae in Pacific Northwest Apple Orchards’, Journal of Economic Entomology, 98, 1459 1468. Arthurs, S.P., Lacey, L.A., and Behle, R.W. (2006), ‘Evaluation of Spray-Dried Lignin-Based Formulations and Adjuvants as Ultraviolet Light Protectants for the Granulovirus of the Codling Moth, Cydia pomonella (L)’, Journal of Invertebrate Pathology, 93, 88 95. Arthurs, S.P., Hilton, R., Knight, A.L., and Lacey, L.A. (2007a), ‘Evaluation of the Pear Ester Kairomone as a Formulation Additive for the Granulovirus of Codling Moth, Cydia pomonella (Lepidoptera: Tortricidae) in Pome Fruit’, Journal of Economic Entomology, 100, 702 709. Arthurs, S.P., Lacey, L.A., and Miliczky, E.R. (2007b), ‘Evaluation of the Codling Moth Granulovirus and Spinosad for Codling Moth Control and Impact on Non-Target Species in Pear Orchards’, Biological Control, 49, 99 109. Asano, S. (2005), ‘Ultraviolet Protection of a Granulovirus Product Using Iron Oxide’, Applied Entomology and Zoology, 40, 359 364. Asquith, D., Croft, B.A., Hoyt, S.C., Glass, E.H., and Rice, R.E. (1980), ‘The Systems Approach and General Accomplishments toward Better Insect Control in Pome and Stone Fruits’, in New Technology of Pest Control, ed. C.B. Huffaker, New York: Wiley, pp. 249 317. Asser-Kaiser, S., Fritsch, E., Undorf-Spahn, K., Kienzle, J., Eberle, K.E., Gund, N.A., Reineke, A., Zebitz, C.P.W., Heckel, D.G., Huber, J., and Jehle, J.A. (2007), ‘Rapid Emergence of Baculovirus Resistance in Codling Moth due to Dominant, Sex Linked Inheritance’, Science, 317, 1916 1918.
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Audemard, H. (1987), ‘Lutte Biologique et Inte´gre´e en Vergers de Pommiers, Poiriers et Abricotiers’, Entomophaga, 32, 59 71. Audemard, H., Burgerjon, A., Baudry, O., Bergere, D., Breniaux, D., Delay, J.C., Desvaux, R., Formantin, C., Gendrier, J.-P., and Tarbouriech, M.F. (1992), ‘Cent Essais de Lutte Contre la Carpocapse Cydia pomonella L. en Verger de Pommiers avec la Carpovirusine, une Preparation de Virus de la Granulose’, Acta Phytopathologica et Entomologica Hungarica, 27, 45 49. Ballard, J., Ellis, D.J., and Payne, C.C. (2000a), ‘The Role of Formulation Additives in Increasing the Potency of Cydia pomonella Granulovirus for Codling Moth Larvae, in Laboratory and Field Experiments’, Biocontrol Science and Technology, 10, 627 640. Ballard, J., Ellis, D.J., and Payne, C.C. (2000b), ‘Uptake of Granulovirus from the Surface of Apples and Leaves by First Instar Larvae of the Codling Moth Cydia pomonella L. (Lepidoptera: Olethreutidae)’, Biocontrol Science and Technology, 10, 617 625. Barnes, M.M. (1991), ‘Tortricids in Pome and Stone Fruits, Codling Moth Occurrence, Host Race Formation and Damage’, in Tortricid Pests, their Biology, Natural Enemies and Control, eds. L.P.S. van der Geest and H.H. Evenhuis, Amsterdam, The Netherlands: Elsevier, pp. 313 327. 656 L.A. Lacey et al.
Begon, M., Sait, S.M., and Thompson, D.J. (1999), ‘Host-Pathogen-Parasitoid Systems’, in Theoretical Approaches to Biological Control, eds. B.A. Hawkins and H.V. Cornell, Cambridge: Cambridge University Press, pp. 327 348. Biache, G., Guillon, M., and Quenin, H. (1998a), ‘Biological Control of Cydia pomonella with ‘‘CarpovirusineReg’’. Trial Results’, Mededelingen Faculteit Landbouwkundige en Toegrpaste biologische Wetenschappen, Universiteit Gent, 63, 455 459. Biache, G., Severini, M., Guillon, M., and Quenin, H. (1998b), ‘Traitements avec la Granulose Effets Secondaires sur le Carpocapsae’, Phytoma, 504, 43 44. Biache, G., Perchat, S., Quenin, H., and Aupinel, P. (1999), ‘La Granulose du Carpocapsae, une Me´thode de Detection de la Maladie Virale par Amplification Ge´nomique’, Phytoma, 514, 27 33. Blommers, L.H.M. (1994), ‘Integrated Pest Management in European Apple Orchards’, Annual Review of Entomology, 39, 213 241. Blommers, L., Vaal, F., Freriks, J., and Helsen, H. (1987), ‘Three Years of Specific Control of Summer Fruit Tortrix and Codling Moth on Apple in The Netherlands’, Journal of Applied Entomology, 104, 353 371. Boivin, T., Chabert d’Hieres, C., Bouvier, J.C., Beslay, D., and Sauphanor, B. (2001), ‘Pleiotropy of Insecticide Resistance in the Codling Moth, Cydia pomonella’, Entomologia Expermentalis et Applicata, 99, 381 386. Boivin, T., Bouvier, J.C., Chadoeuf, J., Beslay, D., and Sauphanor, B. (2003), ‘Constraints on Adaptive Mutations in the Codling Moth Cydia pomonella (L.): Measuring Fitness Trade-Offs and Natural Selection’, Heredity, 90, 107 113. Brain, P., and Glen, D.M. (1989), ‘A Model of the Effect of Codling Moth Granulosis Virus on Cydia pomonella’, Annals of Applied Biology, 115, 129 140. Brassel, J. (1978), ‘Entwicklung von Methoden fur die Produktion eines Granulosis-virus-Praparates zur mikrobiologischen Bekampfung des Apfelwicklers, Laspeyresia pomonella (L.) (Lep., Tortricidae) und Schatzung der Produktionskosten’, Mitteilungen Schweizerischen Entomolo- gischen Gesellschaft, 51, 155 211. Brooks, W.M. (1993), ‘Host-Parasitoid-Pathogen Interactions’, in Parasites and Pathogens of Insects. Vol. 2: Pathogens, eds. N.E. Beckage, S.N. Thompson and B.A. Federici, San Diego, CA: Academic Press, pp. 231 272. Brown, M.W., and Tworkoski, T. (2004), ‘Pest Management Benefits of Compost Mulch in Apple Orchards’, Agriculture, Ecosystems and Environment, 103, 465 472. Bull, D.L., Ridgway, R.L., House, V.S., and Pryor, N.W. (1976), ‘Improved Formulations of the Heliothis Nuclear Polyhedrosis Virus’, Journal of Economic Entomology, 69, 731 736. Burgerjon, A. (1986), ‘Recent Experiences in the Use of the Codling Moth (Cydia pomonella L.) Granulosis Virus in Europe’, in Proceedings of the IV International Colloquium on Invertebrate Pathology, pp. 102 105. Burges, H.D., and Jones, K.A. (1998), ‘Formulation of Bacteria, Viruses and Protozoa to Control Insects’, in Formulation of Microbial Biopesticides, ed. H.D. Burges, Dordrecht: Kluwer Academic Publishers, pp. 33 127. Camponovo, F., and Benz, G. (1984), ‘Age-Dependent Tolerance to Baculovirus in Last Larval Instars of the Codling Moth, Cydia pomonella L., Induced either for Pupation or for Diapause’, Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Experientia, 40, 938 939. Charmillot, P.J., and Pasquier, D. (2002a), ‘Combinaison de la Technique de Confusion et du Virus de la Granulose contre les Souches Resistantes de Carpocapse Cydia pomonella’, Revue Suisse de Viticulture, Arboriculture et Horticulture, 34, 103 108. Charmillot, P.J., and Pasquier, D. (2002b), ‘Progression de la Resistance du Carpocapse Cydia pomonella aux Insecticides’, Revue Suisse Viticulture, Aboriculture et Horticulture, 34, 95 100. Charmillot, P.J., Mayor, P., Keimer, C., and Schmid, A. (1984), ‘Efficacite´ et Reminence de quelques Insecticides e d’un Virus Applique´s contre le Carpocapsae Cydia pomonella’, Revue Suisse de Viticulture, Arboriculture et Horticulture, 16, 222 228. Charmillot, P.J., Pasquier, D., and Scalo, A. (1998), ‘Le Virus de la Granulose du Carpocapse Cydia pomonella: 2. Efficacite´ en Microparcelles, Re´manence et Roˆle des Adjuvants’, Revue Suisse de Viticulture, Arboriculture et Horticulture, 30, 61 64. Cory, J.S., and Evans, H.F. (2008), ‘Virus’, in Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests (2nd ed.), eds. L.A. Lacey and H.K. Kaya, Dordrecht: Springer, pp. 149 174. Biocontrol Science and Technology 657
Cossentine, J.E., and Jensen, L.B.M. (2004), ‘Persistence of a Commercial Codling Moth Granulovirus Product on Apple Fruit and Foliage’, Journal of the Entomological Society of British Columbia, 101, 87 92. Cossentine, J.E., Jensen, L.B., and Deglow, E.K. (2003), ‘Strategy for Orchard Use of Bacillus thuringiensis while Minimizing Impact on Choristoneura rosaceana Parasitoids’, Entomologia Experimentalis et Applicata, 109, 205 210. Cossentine, J.E., Jensen, L.B.M., and Eastwell, K.C. (2005), ‘Incidence and Transmission of a Granulovirus in a Large Codling Moth [Cydia pomonella L. (Lepidoptera: Tortricidae)] Rearing Facility’, Journal of Invertebrate Pathology, 90, 187 192. Couch, T.L., and Ignoffo, C.M. (1981), ‘Formulation of Insect Pathogens’, in Microbial Control of Pests and Plant Diseases 1970 1980, ed. H.D. Burges, London: Academic Press, pp. 621 634. Crook, N.E. (1986), ‘Characterization and Genetics of Cydia pomonella Granulosis Virus’, in Proceedings of the IV International Colloquium on Invertebrate Pathology,pp.84 86. Crook, N., and Winstanley, D. (1990), ‘CpGV Molecular Biology and Prospects for Genetic Engineering’, in Proceedings of the Vth International Colloquium on Invertebrate Pathology and Microbial Control, pp. 434 438. Crook, N.E., Spencer, R.A., Payne, C.C., and Leisy, D.J. (1985), ‘Variation in Cydia pomonella Granulosis Virus Isolates and Physical Maps of the DNA from Three Variants’, Journal of General Virology, 66, 2423 2430. Crook, N.E., James, J.D., Smith, I.R.L., and Winstanley, D. (1997), ‘Comprehensive Physical Map of the Cydia pomonella Granulovirus Genome and Sequence Analysis of the Granulin Gene Region’, Journal of General Virology, 78, 965 974. Cross, J.V., Solomon, M.G., Chandler, D., Jarrett, P., Richardson, P.N., Winstanley, D., Bathon, H., Huber, J., Keller, B., Langenbruch, G.A., and Zimmermann, G. (1999), ‘Biocontrol of Pests of Apples and Pears in Northern and Central Europe: 1. Microbial Agents and Nematodes’, Biocontrol Science and Technology, 9, 125 149. DeBach, P. (1964), Biological Control of Insect Pests and Weeds, London: Chapman & Hall, p. 844 Dickler, E. (1978), ‘Influence of Beneficial Arthropods on the Codling Moth in an Orchard with Green Covered and Clean Cultivated Soil’, Mitteilungen aus der Biologischen Bundesanstalt fur Land und Forstwirtschaft, 1978, 16 18. Dickler, E., and Huber, J. (1986), ‘Modifizierte Strategie bei der Verwendung des Apelwickler- granulosevirus’, IOBC/WPRS Bulletin, 9, 112 115. Do¨ller, G., and Huber, J. (1983), ‘Sicherheitsstudie zur Prufung einer Vermehrung des Granulosevirus aus Laspeyresia pomonella in Saugern’, Zeitschrift fur Angewandte Entomologie, 95, 64 69. Dunley, J.E., and Welter, S.C. (2000), ‘Correlated Insecticide Cross-Resistance in Azinphosmethyl Resistant Codling Moth (Lepidoptera: Tortricidae)’, Journal of Economic Entomology, 93, 955 962. Eastwell, K.C., Cossentine, J.E., and Bernardy, M.G. (1999), ‘Characterisation of Cydia pomonella Granulovirus from Codling Moths in a Laboratory Colony and in Orchards of British Columbia’, Annals of Applied Biology, 134, 285 291. Eberle, K.E., and Jehle, J.A. (2006), ‘Field Resistance of Codling Moth against Cydia pomonella Granulovirus (CpGV) is Autosomal and Incompletely Dominant Inherited’, Journal of Inverte- Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 brate Pathology, 93, 201 206. Eberle, K.E., Asser-Kaiser, S., Sayed, S.M., Nguyen, H.T., and Jehle, J.A. (2008), ‘Overcoming the Resistance of Codling Moth against Conventional Cydia pomonella Granulovirus (CpGV-M) by a New Isolate CpGV-I12’, Journal of Invertebrate Pathology, 98, 293 298. Epstein, D.L., Zack, R.S., Brunner, J.F., Gut, L., and Brown, J.J. (2000), ‘Effects of Broad-Spectrum Insecticides on Epigeal Arthropod Biodiversity in Pacific Northwest Apple Orchards’, Environ- mental Entomology, 29, 340 348. Epstein, D.L., Zack, R.S., Brunner, J.F., Gut, L., and Brown, J.J. (2001), ‘Ground Beetle Activity in Apple Orchards under Reduced Pesticide Management’, Biological Control, 21, 97 104. Etzel, L.K., and Falcon, L.A. (1976), ‘Studies on the Transovum and Transstadial Transmission of a Granulosis Virus of the Codling Moth’, Journal of Invertebrate Pathology, 27, 13 26. Falcon, L.A., and Berlowitz, A. (1986), ‘Experiences Field-Testing Codling Moth Granulosis Virus in the Pacific Rim Countries’, in Proceedings of the IV International Colloquium on Invertebrate Pathology,pp.99 101. 658 L.A. Lacey et al.
Falcon, L.A., and Huber, J. (1991), ‘Biological Control of the Codling Moth’, in Tortricid Pests, their Biology, Natural Enemies and Control, eds. L.P.S. van der Geest and H.H. Evenhuis, Amsterdam: Elsevier, pp. 355 369. Falcon, L.A., Kane, W.R., and Bethel, R.S. (1968), ‘Preliminary Evaluation of a Granulosis Virus for Control of the Codling Moth’, Journal of Economic Entomology, 61, 1208 1213. Farrar, R.R., Shapiro, M., and Javaid, I. (2003), ‘Photostabilized Titanium Dioxide and a Fluorescent Brightener as Adjuvants for a Nucleopolyhedrovirus’, BioControl, 48, 543 560. Federici, B.A. (1986), ‘Ultrastructure of Baculoviruses’, in The Biology of Baculoviruses. Vol. I Biological Properties and Molecular Biology, eds. R.R. Granados and B.A. Federici, Boca Raton, FL: CRC Press, pp. 61 88. Federici, B.A. (1997), ‘Baculovirus Pathogenesis’, in The Baculoviruses, ed. L.K. Miller, New York: Plenum Press, pp. 33 59. Fitzgerald, J.D., and Solomon, M.G. (2004), ‘Can Flowering Plants Enhance Numbers of Beneficial Arthropods in UK Apple and Pear Orchards?’, Biocontrol Science and Technology, 14, 291 300. Fritsch, E., and Huber, J. (1985), ‘Inaktivierung von Apfelwickler-Granuloseviren durch UV- Strahlung und Temperatur’, Nachrichtenblat des Deutschen Pflanzenschutzdienstes, 37, 84 88. Fritsch, E., Huber, J., and Backhaus, H. (1990), ‘CpGV as a Tool in the Risk Assessment of Genetically Engineered Baculoviruses’, in Proceedings of the Vth International Colloquium on Invertebrate Pathology and Microbial Control, pp. 439 443. Fritsch, E., Undorf-Spahn, K., Kienzle, J., Zebitz, C.P.W., and Huber, J. (2005), ‘Apfelwickler Granulovirus: Erste Hinweise auf Unterschiede in der Empfindlichkeit lokaler Apfelwickler Populationen’, Nachrichtenblat des Deutschen Pflanzenschutzdienstes, 57, 29 34. Geissler, K. (1994), ‘Eignung des Granulose-Virus des Apfelwicklers (Cydia pomonella L.) zur Bekampfung des Erbsenwicklers (Cydia nigricana Steph.)’, Archives of Phytopathology and Plant Protection, 29, 191 194. Glen, D.M., and Clark, J.. (1985), ‘Death of Cydia pomonella Larvae and Damage to Apple Fruit, after Field Application of Codling Moth Granulosis Virus’, Entomologia Expermentalis et Applicata, 38, 93 96. Glen, D.M., and Payne, C.C. (1984), ‘Production and Field Evaluation of Codling Moth Granulosis Virus for Control of Cydia pomonella in the United Kingdom’, Annals of Applied Biology, 104, 87 98. Glen, D.M., Wiltshire, C.W., Milsom, N.F., and Brain, P. (1984), ‘Codling Moth Granulosis Virus: Effects of its Use on Some other Orchard Arthropods’, Annals of Applied Biology, 104, 99 106. Gro¨ner, A. (1986), ‘Specificity and Safety of Baculoviruses’, in The Biology of Baculoviruses, Vol. I, Biological Properties and Molecular Biology, eds. R.R. Granados and B.A. Federici, Boca Raton, FL: CRC Press, pp. 177 202. Gro¨ner, A. (1990), ‘Safety to Nontarget Invertebrates of Baculoviruses’, in Safety of Microbial Insecticides, eds. M. Laird, L.A. Lacey and E.W. Davidson, Boca Raton, FL: CRC Press, pp. 135 147. Gro¨ner, A., Huber, J., Krieg, A., and Pinsdorf, W. (1978), ‘Bienenprufung von zwei Baculovirus- Praparaten’, Nachrichtenblat des Deutschen Pflanzenschutzdienstes, 30, 39 41. Guillon, M., and Biache, G. (1995), ‘IPM Strategies for Control of Codling Moth (Cydia pomonella
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 L.) (Lepidoptera Olethreutidae) Interest of CmGV for Long Term Biological Control of Pest Complex in Orchards’, Mededelingen Faculteit Landbouwkundige Universteit Gent, 60, 695 705. Gurr, G.M., Thwait, W.G., and Nicol, H.I. (1999), ‘Field Evaluation of the Effects of the Insect Growth Regulator Tebufenozide on Entomophagous Arthropods and Pests of Apples’, Australian Journal of Entomology, 38, 135 140. Harvey, J.P., and Volkman, L.E. (1983), ‘Biochemical and Biological Variation of Cydia pomonella (codling moth) Granulosis Virus’, Virology, 124, 21 34. Helsen, H., Blommers, L., and Vaal, F. (1992), ‘Efficacy and Implementation of Granulosis Virus against Codling Moth in Orchard IPM’, Mededelingen Faculteit Landbouwkundige’, Rijksuniversi- teit Gent, 57, 569 573. Hess, R.T., and Falcon, L.A. (1987), ‘Temporal Events in the Invasion of the Codling Moth, Cydia pomonella, by a Granulosis Virus: An Electron Microscope Study’, Journal of Invertebrate Pathology, 50, 85 105. Hilton, S., and Winstanley, D. (2007), ‘Identification and Functional Analysis of the Origins of DNA Replication in the Cydia pomonella Granulovirus Genome’, Journal of General Virology, 88, 1496 1504. Biocontrol Science and Technology 659
Horton, D.R., Broers, D.A., Lewis, R.R., Granatstein, D., Zack, R.S., Unruh, T.R., Moldenke, A.R., and Brown, J.J. (2003), ‘Effects of Mowing Frequency on Densities of Natural Enemies in Three Pacific Northwest Pear Orchards’, Entomologia Experimentalis et Applicata, 106, 135 145. Huber, J. (1980), ‘Field Persistence of the Codling Moth Granulosis Virus’, Bulletin IOBC/WPRS,3, 58 59. Huber, J. (1981), ‘Apfelwickler-Granulosevirus: Produktion und Biotests’, Mitteilungen der deutschen Gesellschaft fu¨ r allgemeine angewandte Entomologie, 2, 141 145. Huber, J. (1986), ‘Use of Baculoviruses in Pest Management Programs’, in The Biology of Baculoviruses. Vol. II. Practical Application for Insect Control, eds. R.R. Granados and B.A. Federici, Boca Raton, FL: CRC Press, pp. 181 202. Huber, J., and Dickler, E. (1975), ‘Freilandversuche zur Beka¨mpfung des Apfelwicklers, Laspeyresia pomonella (L.) mit Granuloseviren’, Zeitschrift fu¨ r Pflanzenkrankheiten und Pflanzenschutz, 82, 540 546. Huber, J., and Dickler, E. (1977), ‘Codling Moth Granulosis Virus: Its Efficiency in the Field in Comparison with Organophosphorus Insecticides’, Journal of Economic Entomology, 70, 557 561. Huber, B., Nyrop, J.P., Wolf, W., Reissig, H., Agnello, A., and Kovach, J. (1990), ‘Development of a Knowledge-Based System Supporting IPM Decision Making in Apples’, Computers and Electronics in Agriculture, 4, 315 331. Ignoffo, C.M. (1992), ‘Environmental Factors Affecting Persistence of Entomopathogens’, Florida Entomologist, 75, 516 525. Irvin, N.A., Scarratt, S.L., Wratten, S.D., Frampton, C.M., Chapman, R.B., and Tylianakis, J.M. (2006), ‘The Effects of Floral under Stories on Parasitism of Leafrollers (Lepidoptera: Tortricidae) on Apples in New Zealand’, Agricultural and Forest Entomology,8,25 34. Jans, P., and Benz, G. (1985), ‘Weight Increase of Granulosis Virus Infected Allatectomized Larvae of the Codling Moth, Cydia pomonella (L.) (Lep., Tortricidae)’, Mitteilungen der Schweizerischen. Entomologischen Gesellschaft, 58, 341 344. Jaques, R.P. (1985), ‘Stability of Insect Viruses in the Environment’, in Viral Insecticides for Biological Control, eds. K. Maramorosch and K.E. Sherman, New York: Academic Press, pp. 285 360. Jaques, R.P. (1990), ‘Effectiveness of the Granulosis Virus of the Codling Moth in Orchard Trials in Canada’, Proceedings of the Vth International Colloquium on Invertebrate Pathology and Microbial Control, pp. 428 430. Jaques, R.P, MacLellan, C.R., Sanford, K.H., Proverbs, M.D., and Hagley, E.A.C. (1977), ‘Preliminary Orchard Tests on Control of Codling Moth Larvae by a Granulosis Virus’, Canadian Entomologist, 109, 1079 1081. Jaques, R.P., Laing, J.E., MacLellan, C.R., Proverbs, M.D., Sanford, K.H., and Trottier, R. (1981), ‘Apple Orchard Tests on the Efficacy of the Granulosis Virus of the Codling Moth Laspeyresia pomonella (Lep: Olethreutidae)’, Entomophaga, 26, 111 118. Jaques, R.P., Laing, J.E., Laing, D.R., and Yu, D.S.K. (1987), ‘Effectiveness and Persistence of the Granulosis Virus of the Codling Moth Cydia pomonella (L.) (Lepidoptera: Olethreutidae) on Apple’, Canadian Entomologist, 119, 1063 1067. Jaques, R.P., Hardman, J., Laing, J., and Smith, R. (1994), ‘Orchard Trials in Canada on Control of Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Cydia pomonella (Lep: Tortricidae) by Granulosis Virus’, Entomophaga, 39, 281 292. Jehle, J.A., Fritsch, E., Nickel, A., Huber, J., and Backhaus, H. (1995), ‘TCl4.7: A Novel Lipidopteran Transposon Found in Cydia pomonella Granulosis Virus’, Virology, 207, 369 379. Jehle, J.A., van der Linden, I.F.A., Backhaus, H., and Vlak, J.M. (1997), ‘Identification and Sequence Analysis of the Integration Site of Transposon TCp3.2 in the Genome of Cydia pomonella granulovirus’, Virus Research, 50, 151 157. Jehle, J.A., Nickel, A., Vlak, J.M., and Backhaus, H. (1998), ‘Horizontal Escape of the Novel Tc1-like Lepidopteran Transposon TCp3.2 into Cydia pomonella Granulovirus’, Journal of Molecular Evolution, 46, 215 224. Jehle, J.A., Fritsch, E., Huber, J., and Backhaus, H. (2003), ‘Intra-Specific and Inter-Specific Recombination of Tortricid-Specific Granuloviruses during Co-Infection in Insect Larvae’, Archives of Virology, 148, 1317 1333. Jehle, J.A., Blissard, G.W., Bonning, B.C., Cory, J.S., Herniou, E.A., Rohrmann, G.F., Theilmann, D.A., Thiem, S.M., and Vlak, J.M. (2006), ‘On the Classification and Nomenclature of Baculoviruses: A Proposal for Revision’, Archives of Virology, 151, 1257 1266. 660 L.A. Lacey et al.
Jones, K.A., and Burges, H.D. (1998), ‘Principles of Formulation’, in Formulation of Microbial Biopesticides, ed. H.D. Burges, Dordrecht: Kluwer Academic Publishers, pp. 7 30. Kang, W., Crook, N.E., Winstanley, D., and O’Reilly, D.R. (1997), ‘Complete Sequence and Transposon Mutagenesis of the BamHI J Fragment of Cydia pomonella Granulosis Virus’, Virus Genes, 14, 131 136. Kang, W., Tristem, M., Maeda, S., Crook, N.E., and O’Reilly, D.R. (1998), ‘Identification and Characterization of the Cydia pomonella Granulovirus Cathepsin and Chitinase Genes’, Journal of General Virology, 79, 2283 2292. Kaya, H.K., and Lacey, L.A. (2007), ‘Introduction to Microbial Control’, in Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests (2nd ed.), eds. L.A. Lacey and H.K. Kaya, Dordrecht: Springer, pp. 3 7. Kaya, H.K., Joos, J.L., Falcon, L.A., and Berlowitz, A. (1984), ‘Suppression of the Codling Moth (Lepidoptera: Olethreutidae) with the Entomogenous Nematode, Steinernema feltiae (Rhabditida: Steinernematidae)’, Journal of Econonomic Entomology, 77, 1240 1244. Keller, S. (1973), ‘Mikrobiologische Beka¨mpfung des Apfelwicklers (Laspeyresia pomonella (L.)) ( Carpocapsa pomonella) mit spezifischem Granulosisvirus’, Zeitschrift fur Angewandte Entomo- logie, 73, 137 181. Kienzle, J., Gernoth, H., Zebitz, C.P.W., and Huber, J. (2003a), ‘Codling Moth Granulovirus An Efficient Tool for Codling Moth Control’, Bulletin OILB/SROP, 26, 249 253. Kienzle, J., Schulz, C., Zebitz, C.P.W., and Huber, J. (2003b), ‘Codling Moth Granulovirus as a Tool for Resistance Management and Area-Wide Population Control’, Bulletin OILB/SROP, 26, 69 74. Kienzle, J., Schulz, C., Zebitz, C.P.W., and Huber, J. (2003c), ‘Persistence of the Biological Effect of Codling Moth Granulovirus in the Orchard A Preliminary Field Trial’, Bulletin OILB/SROP, 26, 245 248. Krieg, A., Gro¨ner, A., Huber, J., and Zimmermann, G. (1981), ‘Inaktivierung von verschiedenen Insektenpathogenen durch ultraviolette Strahlen’, Zeitschrift Pflanzenkrankheiten Pflschut- zenschutz, 88, 38 48. Kundu, J.K., Stara?, J., Kocourek, F., and Pultar, O. (2003), ‘Polymerase Chain Reaction Assay for Cydia pomonella Granulovirus Detection in Cydia pomonella Population’, Acta Virologica, 47, 153 157. Lacey, L.A. (2008), ‘Resistance in Cydia pomonella to the Codling Moth Granulovirus in Europe: Could it Happen Here?’, in Proceedings of the Western Orchard Pest and Disease Management Conference,pp.12 13. Lacey, L.A., and Arthurs, S.P. (2005), ‘New Method for Testing Solar Sensitivity of Commercial Formulations of the Granulovirus of Codling Moth (Cydia pomonella, Tortricidae: Lepidoptera)’, Journal of Invertebrate Pathology, 90, 85 90. Lacey, L.A., and Shapiro-Ilan, D.I. (2008), ‘Microbial Control of Insect Pests in Temperate Orchard Systems: Potential for Incorporation into IPM’, Annual Review of Entomology, 53, 121 144. Lacey, L.A., and Siegel, J.P. (2000), ‘Safety and Ecotoxicology of Entomopathogenic Bacteria’, in Entomopathogenic Bacteria: from Laboratory to Field Application, eds. J.F. Charles, A. Dele´cluse and C. Nielsen-LeRoux, Dordrecht: Kluwer Academic Publishers, pp. 253 273. Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Lacey, L.A., and Unruh, T.R. (2005), ‘Biological Control of Codling Moth (Cydia pomonella, Tortricidae: Lepidoptera) and its Role in Integrated Pest Management, with Emphasis on Entomopathogens’, Vedalia, 12, 33 60. Lacey, L.A., Frutos, R., Kaya, H.K., and Vail, P. (2001), ‘Insect Pathogens as Biological Control Agents: Do They Have a Future?’, Biological Control, 21, 230 248. Lacey, L.A., Vail, P.V., and Hoffmann, D.F. (2002), ‘Comparative Activity of Baculoviruses against the Codling Moth, Cydia pomonella, and Three other Tortricid Pests if Tree Fruit’, Journal of Invertebrate Pathology, 80, 64 68. Lacey, L.A., Arthurs, S.P., Knight, A., Becker, K., and Headrick, H. (2004), ‘Efficacy of Codling Moth Granulovirus: Effect of Adjuvants on Persistence of Activity and Comparison with other Larvicides in a Pacific Northwest Apple Orchard’, Journal of Entomological Science, 39, 500 513. Lacey, L.A., Arthurs, S.P., and Headrick, H. (2005a), ‘Comparative Activity of the Codling Moth Granulovirus against Grapholita molesta and Cydia pomonella (Lepidoptera: Tortricidae)’, Journal of the Entomological Society of British Columbia, 102, 79 80. Biocontrol Science and Technology 661
Lacey, L.A., Neven, L.G., Headrick, H.L., and Fritts, R. Jr. (2005b), ‘Factors Affecting Entomopathogenic Nematodes (Steinernematidae) for Control of Overwintering Codling Moth (Lepidoptera: Tortricidae) in Fruit Bins’, Journal of Economic Entomology, 98, 1863 1869. Lacey, L.A., Arthurs, S.P., Unruh, T.R., Headrick, H., and Fritts, R. Jr. (2006), ‘Entomopathogenic Nematodes for Control of Codling Moth (Lepidoptera: Tortricidae) in Apple and Pear Orchards: Effect of Nematode Species and Seasonal Temperatures, Adjuvants, Application Equipment and Post-Application Irrigation’, Biological Control, 37, 214 223. Lacey, L.A., Arthurs, S.P., Knight, A., and Huber, J. (2007), ‘Microbial Control of Lepidopteran Pests of Apple Orchards’, in Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests (2nd ed.), eds. L.A. Lacey and H.K. Kaya, Dordrecht: Springer, pp. 527 546. Lacey, L.A., Headrick, H.L., and Arthurs, S.P. (2008), ‘The Effect of Temperature on the Long-Term Storage of Codling Moth Granulovirus Formulations’, Journal of Economic Entomology, 101, 288 294. Laing, D.R., and Jaques, R.P. (1980), ‘Codling Moth: Techniques for Rearing Larvae and Bioassaying Granulosis Virus’, Journal of Economic Entomology, 73, 851 853. LeRoux, E.J. (1961), ‘Effects of Modified and Commercial Spray Programs on the Fauna of Apple Orchards in Quebec’, Annals of the Entomological Society of Quebec,6,87 121. Light, D.M. (2007), ‘Experimental Use of the Micro-Encapsulated Pear Ester Kairomone for Control of Codling Moth, Cydia pomonella (L.) in Walnuts’, IOBC WPRS Bulletin, 30, 21. Lu, C., Barr, D.B., Pearson, M.A., and Waller, L.A. (2008), ‘Dietary Intake and its Contribution to Longitudinal Organophosphorus Pesticide Exposure in Urban/Suburban Children’, Environmental Health Perspectives, 116, 537 542. Luque, T., Finch, R., Crook, N., O’Reilly, D.R., and Winstanley, D. (2001), ‘The Complete Sequence of the Cydia pomonella Granulovirus Genome’, Journal of General Virology, 82, 2531 2547. MacHardy, W.E. (2000), ‘Current Status of IPM in Apple Orchards’, Crop Protection, 19, 801 806. Madsen, H.F., and Madsen, B.J. (1982), ‘Populations of Beneficial and Pest Arthropods in an Organic and a Pesticide Treated Apple Orchard in British Columbia’, Canadian Entomologist, 114, 1083 1088. Mathews, C.R., Bottrell, D.G., and Brown, M.W. (2004), ‘Habitat Manipulation of the Apple Orchard Floor to Increase Ground-Dwelling Predators and Predation of Cydia pomonella (L.) (Lepidoptera: Tortricidae)’, Biological Control, 30, 265 273. Miliczky, E.R., Calkins, C.O., and Horton, D.R. (2000), ‘Spider Abundance and Diversity in Apple Orchards under Three Insect Pest Management Programmes in Washington State, USA’, Agricultural and Forest Entomology, 2, 203 215. Min˜arro, M., and Dapena, E. (2000), ‘Control de Cydia pomonella (L.) (Lepidoptera: Tortricidae) con Granulovirus y Confusion Sexual en Plantaciones de Manzano de Asturias. Boletı´n de Sanidad Vegetal’, Plagas, 26, 305 316. Min˜arro, M., and Dapena, E. (2003), ‘Effects of Groundcover Management on Ground Beetles (Coleoptera: Carabidae) in an Apple Orchard’, Applied Soil Ecology, 23, 111 117. Naser, W.L. (1986), ‘Establishment of a Cydia pomonella Granulosis Virus in vitro Replication System’, Fourth International Colloquium of Invertebrate Pathology, Wageningen, The Netherlands, Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 pp. 91 101. Naser, W.L., Miltenburger, J.P., Harvey, J.P., Huber, J., and Huger, A.M. (1984), ‘In vitro Replication of the Cydia pomonella (Codling Moth) Granulosis Virus’, FEMS Microbiology Letters, 24, 117 121. Nicholas, A.H., Thwaite, W.G., and Spooner-Hart, R.N. (1999), ‘Arthropod Abundance in an Australian Apple Orchard under Mating Disruption and Supplementary Insecticide Treatments for Codling Moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae)’, Australian Journal of Entomology, 38, 23 29. Pasqualini, E., Schmidt, S., Espinha, I., Civolani, S., DeCristofaro, A., Molinari, F., Villa, M., Ladurner, E., Sauphanor, B., and Ioriatti, C. (2005), ‘Effects of the Kairomone Ethyl (2E, 4Z)-2,4- Decadienoate (DA 2313) on the Oviposition Behaviour of Cydia pomonella: Preliminary Investigations’, Bulletin of Insectology, 58, 119 124. Pasquier, D., and Charmillot, P.J. (1998), ‘Le Virus de la Granulose du Carpocapse Cydia pomonella. 3. Essai Pratique de Longue Dure´e’, Revue Suisse de Viticulture, d’Arboriculture et d’ Horticulture, 30, 185 187. 662 L.A. Lacey et al.
Payne, C.C. (1981), ‘The Susceptibility of the Pea Moth, Cydia nigricana, to Infection by the Granulosis Virus of the Codling Moth, Cydia pomonella’, Journal of Invertebrate Pathology, 38, 71 77. Prokopy, R.J., Cooley, D.R., Autio, W.R., and Coli, W.M. (1994), ‘Second-level Integrated Pest Management in Commercial Apple Orchards’, American Journal of Alternative Agriculture, 9, 148 156. Prokopy, R.J., Mason, J.L., Christie, M., and Wright, S.E. (1996), ‘Arthropod Pest and Natural Enemy Abundance under Second-Level Versus First-Level Integrated Pest Management Practices in Apple Orchards: A 4-year Study’, Agriculture, Ecosystems and Environment, 57, 35 47. Pszczolkowski, M.A., and Brown, J.J. (2004), ‘Enhancement of Spinosad Toxicity to Cydia pomonella Neonates by Monosodium Glutamate Receptor Agonist’, Phytoparasitica, 32, 342 350. Pszczolkowski, M.A., Matos, L., Zahand, A., and Brown, J.J. (2002), ‘Effect of Monosodium Glutamate on Apple Leaf Consumption by Codling Moth Larvae’, Entomologia Expermentalis et Applicata, 103, 91 98. Rashid, T., Johnson, D.T., Steinkraus, D.C., and Rom, C.R. (2001), ‘Effects of Microbial, Botanical and Synthetic Insecticides on ‘‘Red Delicious’’ Apples in Arkansas’, HortTechnology, 11, 615 621. Reiser, M., Gro¨ner, A., and Sander, E. (1993), ‘Cryptophlebia leucotreta (Lep.: Tortricidae) A Promising Alternate Host for Mass Production of the Cydia pomonella Granulosis Virus (CpGV) for Biological Pest Control’, Zeitschrift Pflanzenkrankheiten Pflanzenschutz, 100, 586 598. Reyes, M., Franck, P., Charmillot, P.J., Ioriatti, C., Olivares, J., Pasqualini, E., and Sauphanor, B. (2007), ‘Diversity of Insecticide Resistance Mechanisms and Spectrum in European Populations of the Codling Moth, Cydia pomonella’, Pest Management Science, 63, 890 902. Rezapanah, M.R., Assady, H.B., Esmaili, M., and Ghanbalani, G.N. (1996), ‘Effects of Solar Radiation on Efficacy of Cydia pomonella Granulosis Virus’, Applied Entomology and Phyto- pathology, 63, 26 31. Rezapanah, M., Kharrazi-Pakdel, A., Kamali, K., and Huber, J. (2002), ‘Survey on Natural Occurrence of Cydia pomonella Granulovirus in Apple Orchards of Iran’, Applied Entomology and Phytopathology, 69, 49 55 (in Persian). Richards, M.G. (1986), ‘Aspects of the Commercialization of Codling Moth Granulosis Virus’, in Proceedings of the IV International Colloquium on Invertebrate Pathology,pp.95 98. Riddick, E.W., and Mills, N.J. (1995), ‘Seasonal Activity of Carabids (Coleoptera: Carabidae) Affected by Microbial and Oil Insecticides in an Apple Orchard in California’, Environmental Entomology, 24, 361 366. Saik, J.E., Lacey, L.A., and Lacey, C.M. (1990), ‘Safety of Microbial Control Agents to Domestic Animals and Vertebrate Wildlife’, in Safety of Microbial Insecticides, eds. M. Laird, L.A. Lacey and E.W. Davidson, Boca Raton, FL: CRC Press, pp. 115 132. Sauphanor, B., Bouvier, J.C., and Brosse, V. (1998), ‘Spectrum of Insecticide Resistance in Cydia pomonella (Lepidoptera: Tortricidae) in Southeastern France’, Journal of Economic Entomology, 91, 1225 1231. Sauphanor, B., Berling, M., Toubon, J.F., Reyes, M., and Delnatte, J. (2006), ‘Carpocapse des Pommes: Cas de Re´sistance aux Virus de la Granulose dans le Sud-Est’, Phytoma, 590, 24 27. Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Sheppard, R.F., and Stairs, G.R. (1976), ‘Effects of Dissemination of Low Dosage Levels of a Granulosis Virus in Populations of the Codling Moth’, Journal of Economic Entomology, 69, 583 586. Sheppard, R.F., and Stairs, G.R. (1977), ‘Dosage-Mortality and Time-Mortality Studies of a Granulosis Virus in a Laboratory Strain of the Codling Moth, Laspeyresia pomonella’, Journal of Invertebrate Pathology, 29, 216 221. Skrzecz, I. (2000), ‘Preliminary Results of Experiments for the Use of Baculoviruses in Polish Forestry’, Bulletin-OILB/SROP, 23, 243 247. Simon, S., Defrance, H., and Sauphanor, B. (2007), ‘Effect of Codling Moth Management on Orchard Arthropods’, Agriculture, Ecosystems and Environment, 122, 340 348. Stairs, G.R., Parrish, W.B., Briggs, J.D., and Allietta, M. (1966), ‘Fine Structure of a Granulosis Virus of the Codling Moth’, Virology, 30, 583 584. Stara´, J., and Kocourek, F. (2003), ‘Evaluation of the Efficacy of Cydia pomonella Granulovirus (CpGV) to Control the Codling Moth (Cydia pomonella L., Lep.: Tortricidae) in Field Trials’, Plant Protection Science, 39, 117 125. Biocontrol Science and Technology 663
Steineke, S.B., and Jehle, J.A. (2004), ‘Investigating the Horizontal Transmission of the Cydia pomonella Granulovirus (CpGV) in a Model System’, Biological Control, 30, 538 545. Stephens, M.J., France, C.M., Wratten, S.D., and Frampton, C. (1998), ‘Enhancing Biological Control of Leafrollers (Lepidoptera: Tortricidae) by Sowing Buckwheat (Fagopyrum esculentum) in an Orchard’, Biocontrol Science and Technology, 8, 547 558. Suckling, D.M., Walker, J.T.S., and Wearing, C.H. (1999), ‘Ecological Impact of Three Pest Management Systems in New Zealand Apple Orchards’, Agriculture, Ecosystems and Environment, 73, 129 140. Tanada, Y. (1964), ‘A Granulosis Virus of the Codling Moth, Carpocapsae pomonella (Linnaeus) (Olethreutidae, Lepidoptera)’, Journal Insect Pathology, 6, 378 380. Tanada, Y., and Hess, R.T. (1991), ‘Baculoviridae, Granulosis Viruses’, in Atlas of Invertebrate Viruses, eds. J.R. Adams and J.R. Bonami, Boca Raton, FL: CRC Press, pp. 227 257. Tanada, Y., and Leutenegger, R. (1968), ‘Histopathology of a Granulosis-Virus Disease of the Codling Moth, Carpocapsae pomonella’, Journal of Invertebrate Pathology, 10, 39 47. Theilmann, D.A., Blissard, G.W., Bonning, B., Jehle, J., O’Reilly, D.R., Rohrmann, G.F., Theim, S., and Vlak, J. (2005), ‘Family Baculoviridae’, in Virus Taxonomy, Eighth Report of the International Committee on Virus Taxonomy, eds. C.M. Fauquet, M.A. Mayo, M. Maniloff, U. Desselberger and L.A. Ball, San Diego, CA: Elsevier Press, pp. 177 185. Trematerra, P., Borserio, E., and Tonesi, R. (1996), ‘Integrazione di Virus della Granulose e Confusione nella lotta a Cydia pomonella L’, Informatore Fitopatologico, 46, 62 64. Trematerra, P., Manzini, M., and Tanno, M. (1997), ‘Efficacia del Virus della Granulosi nel Controllo di Cydia pomonella in un Mileto a Cultivar Plurime Condotto ad Agricultura Biologica’, Informatore Fitopatologico, 47, 61 64. Vail, P.V., Barnett, W., Cowan, D.C., Sibbett, S., Beede, R., and Tebbets, J.S. (1991), ‘Codling Moth (Lepidoptera: Tortricidae) Control on Commercial Walnuts with a Granulosis Virus’, Journal of Economic Entomology, 84, 1448 1453. van den Bosch, R., Messenger, P.S., and Gutierrez, A.P. (1982), An Introduction to Biological Control, New York: Plenum Press, p. 247. Vincent, C.M., Andermatt, M., and Vale´ro, J. (2007), ‘Madex and Virosoft, Viral Biopesticides for Codling Moth Control’, in Biological Control: A Global Perspective, eds. C. Vincent, M.S. Goettel and G. Lazarovits, Wallingford, Oxfordshire: CAB International, pp. 336 343. Warner, G. (2007), ‘Wake-up Call for Virus Users’, Good Fruit Grower, 58 (17), 14 15. Wearing, C.H. (1993), ‘Control of Codling Moth with a Commercial Preparation of Granulosis Virus’, in Proceedings of the 46th New Zealand Plant Protection Conference, pp. 146 151. Williams, T., Valle, J., and Vinuela, E. (2003), ‘Is the Naturally Derived Insecticide Spinosad† Compatible with Insect Natural Enemies?’, Biocontrol Science and Technology, 13, 459 475. Winstanley, D., and Crook, N.E. (1993), ‘Replication of Cydia pomonella Granulosis Virus in Cell Cultures’, Journal of General Virology, 74, 1599 1699. Winstanley, D., Jarrete, P.J., and Morgan, A.W. (1998), ‘The Use of Transgenic Biological Control Agents to Improve their Performance in the Management of Pests’, in Biotechnology in Crop Protection: Facts and Fallacies, ed. B.R. Kerry, Proceedings of the British Crop Protection Council Symposium No. 71, pp. 37 44.
Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Zingg, D., and Kessler, P. (2008), ‘Madex plus and Madex I12 Break Virus Resistance of Codling Moth’, Andermatt Group Publication, 15, 7 10.