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Diptera: Tephritidae) Cesar Rodriguez-Saona,1,2 Charles Vincent,3 Dean Polk,4 and Francis A

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Diptera: Tephritidae) Cesar Rodriguez-Saona,1,2 Charles Vincent,3 Dean Polk,4 and Francis A Journal of Integrated Pest Management PROFILES A Review of the Blueberry Maggot Fly (Diptera: Tephritidae) Cesar Rodriguez-Saona,1,2 Charles Vincent,3 Dean Polk,4 and Francis A. Drummond5 1Department of Entomology, Rutgers University, P.E. Marucci Center, 125A Lake Oswego Rd., Chatsworth, NJ 08019. 2Corresponding author, e-mail: [email protected]. 3Horticultural Research and Development Centre, Agriculture and Food-Agri Canada, 430 Gouin Blvd., Saint-Jean-sur-Richelieu, Quebec Canada J3B 3E6. 4Department of Agricultural and Resource Management Agents Rutgers Fruit Research and Extension Center, 283 Route 539, Cream Ridge, NJ 08514. 5School of Biology and Ecology, University of Maine, 305 Deering Hall, Orono, ME 04469. J. Integ. Pest Mngmt. (2015) 15(1): 11; DOI: 10.1093/jipm/pmv010 ABSTRACT. Native to North America, the blueberry maggot fly, Rhagoletis mendax Curran (Diptera: Tephritidae), has historically been considered one of the most important insect pests of commercially grown highbush and lowbush blueberries in many parts of the northeastern and north central United States and Canada. Larval infestation results in unmarketable berries owing to a zero-tolerance policy enforced by quarantine regulations for exporting berries to countries outside the United States. To keep berries free from larvae, growers need to maintain an intensive management program that is based mainly on chemical control targeted at adults. Blueberry maggot flies have been largely managed by the use of broad-spectrum insecticides, including organophosphates and carbamates; how- ever, restricted use of these old chemistries has resulted in increased use of “reduced-risk” neonicotinoids. Integrated pest manage- ment programs for blueberry maggot include the use of monitoring tools such as Pherocon-AM sticky traps, site-specific insecticide applications, border sprays, and use of reduced-risk insecticides. The pest status of the blueberry maggot fly in blueberries has changed recently due to the invasion into the continental United States of the spotted wing drosophila, Drosophila suzukii Matsumura, which has now become the main target of insecticide applications, replacing the blueberry maggot. This new invasive pest has disrupted inte- grated pest management programs implemented for blueberry maggot. The present review describes the biology, ecology, crop injury, monitoring tools, and control strategies currently used for blueberry maggot in blueberries, as well as provide a perspective on its pre- sent and potential future pest status. Key Words: Rhagoletis mendax, blueberry, monitoring, management, chemical control Historically, the blueberry maggot fly, Rhagoletis mendax Curran blueberry production in the United States and Canada. However, the (Diptera: Tephritidae), has been considered one of the most serious new invasive pest spotted wing drosophila, Drosophila suzukii insect pests of cultivated highbush (Vaccinium corymbosum L.) and Matsumura (Diptera: Drosophilidae), has recently become the primary lowbush (Vaccinium angustifolium Aiton) blueberries in many parts of target of insecticide sprays in most commercial blueberry farms. In that the eastern United States and Canada (Prokopy and Coli 1978, Neilson context, we provide a perspective on current and future pest status for and Wood 1985, Geddes et al. 1987). Because blueberry maggot larval the blueberry maggot. infestation makes fruit unmarketable, there is a zero tolerance for this pest in most production areas. As a result, strict integrated pest manage- Biology, Identification, and Distribution ment (IPM) programs are practiced and quarantine regulations have Identification. Blueberry maggot adults range in size from 3 to 5 mm been enforced in countries like Canada to prevent the introduction of in length (female 4.75 mm; Fig. 1). The female abdomen is pointed this pest in areas where it is not yet present (Canadian Food Inspection and black with four white cross-bands. The thorax is black with a small, Agency [CFIA] 2014). backward-pointing, white projection (scutellum). The male fly is As the blueberry maggot spends most of its life as a pupa in the soil smaller than the female and has a rounded abdomen with only three and as larvae in well-protected berries, few soft management tactics are white cross-bands. The wings (wingspan 8 mm) of both sexes are available. The main tools available are insecticidal sprays targeted at clear and are patterned with black bands characteristic of many tephritid adults, which is a major challenge for the development of sustainable species. Blueberry maggot adults are identifiable by the characteristic practices in cultivated blueberry. Several features of the blueberry mag- solid “W”or “M” shape mark on their wings (Fig. 1). In most cases, this got biology are constraints from a research standpoint. Blueberry mag- is identical to apple maggot flies, R. pomonella (Fig. 2). Separation of got can be reared (e.g., Neilson 1965), but it cannot be multiplied by these species depends on measurements of wing band ratios, ovipositor rearing. It is predominantly a univoltine insect that must undergo an length, and genitalia (Lathrop and Nickels 1932). Protein variation and obligatory diapause of 120 d (Teixeira and Polavarapu 2005a), which molecular markers can also be used (Berlocher and Bush 1982, Feder also restricts mass rearing. Despite these challenges, the blueberry mag- et al. 1989). Although not as reliable as the former characters, one might got has been the subject of extensive basic and applied research owing assume that if a fly is captured in a commercial blueberry field, then it is to its pest status. For example, in an ecological and evolutionary angle, likely blueberry maggot. However, many blueberry fields in northern the blueberry maggot and its sibling species, such as the apple maggot United States and Canada are often within a short distance of nonman- fly Rhagoletis pomonella Walsh, have been used as model systems for aged apple and wild hawthorn (Crataegus spp.). The distinct wing band the study of sympatric speciation (Feder and Bush 1989). patterns can be used to definitely separate blueberry maggot flies from Literature reviews on the blueberry maggot have been published walnut husk fly (Rhagoletis completa Cresson), cherry fruit fly more than two decades ago by Neilson and Wood (1985) and Geddes (Rhagoletis cingulata Loew; Fig. 2), and black cherry fruit fly et al. (1987). In the present review, we summarize recent advances on (Rhagoletis fausta Osten Sacken). the biology and ecology of the blueberry maggot, as well as on monitor- Larvae (Fig. 3) are pale white and translucent, and their body is con- ing and pre- and postharvest management options. Prior to 2008, the ical, with the anterior end tapered and the posterior end possessing blueberry maggot fly was the main driver of insecticide sprays for paired spiracles. They develop in the host fruit, require three instars, VC The Author 2015. Published by Oxford University Press on behalf of the Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 15, NO. 1 Fig. 3. R. mendax larva in huckleberry, G. baccata, fruit. Fig. 1. Adult of the blueberry maggot fly, R. mendax, with the and attain a final length of 5–6 mm prior to pupation. Burgher- characteristic solid “W” or “M” shape mark on its wings. MacLellan et al. (2009) used real-time polymerase chain reaction (PCR) for molecular identification of larvae in fruit of lowbush blue- berry and Kim et al. (2014) used PCR-restriction fragment length poly- morphism to distinguish larvae and pupae of Drosophila spp. including spotted wing drosophila, D. suzukii. Using cytochrome oxidase I and II, they concluded that it is possible to quickly and reliably distinguish blueberry maggot, apple maggot, black cherry fruit fly, and Drosophila melanogaster Meigen at low cost. Because of its recent economic importance, spotted wing drosophila must be included in the list of tar- geted species. Taxonomy. Within the genus Rhagoletis, blueberry maggot belongs to the pomonella species group together with apple maggot, Rhagoletis zephyria Snow, and Rhagoletis cornivora Bush (Bush 1966, McPheron and Han 1997, Smith and Bush 1997). Despite the fact that flies are smaller and could not oviposit on apple, the first reports of blueberry maggot in eastern North America identified the insect as the apple mag- got based on morphological characteristics (Woods 1914, O’Kane 1914). Later, Curran (1932) recognized blueberry maggot as a new spe- cies based on the shape of the ejaculator apodeme in males. However, the debate on whether to place the blueberry maggot as a new species continued due to inconclusive cross-breeding and host selection studies (Beckwith and Doehlert 1937, Lathrop 1952, Christenson and Foote 1960). In his revision of the genus Rhagoletis, Bush (1966) classified blueberry maggot as a distinct species based on its host range, behavior, and ecology; crossbreeding and oviposition experiments; and small but consistent morphological differences. The fact that blueberry maggot and apple maggot have different host preferences has likely prevented them from interbreeding
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