Journal of Integrated Pest Management PROFILES

A Review of the Blueberry Maggot (Diptera: ) 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, mendax Curran (Diptera: Tephritidae), has historically been considered one of the most important 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 , 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 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 ( 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 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 , 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. . 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 (Diehl and Prokopy 1986); apple maggot uses plants belonging to the family Rosaceae as hosts, while blueberry mag- got uses hosts in the family . Berlocher (1995) found differen- ces in the population structure between these two species. Teixeira and Polavarapu (2002, 2003) even found genetic differences between early and late emerging populations of blueberry maggot in New Jersey. They also found differences in the genetic diversity between wild popu- lations and those from cultivated blueberries, the former having more diverse populations (Teixeira and Polavarapu 2002, 2003), indicative of a small sample of wild individuals colonizing the cultivated blueberries. Life Cycle and Seasonal Biology. The life history and phenology of the blueberry maggot varies according to geographical location. Most populations in North America are univoltine (Lathrop and Nickels 1932), but in Maine, and possibly other locations, 85% of the popula- tion is univoltine, while 10 and 5% of the population spends two and three or even four winters as a pupa (Fig. 4), respectively. In the spring or early summer of the year, just prior or at the time of the beginning of Fig. 2. Rhagoletis spp. wing pattern (adapted from Carroll et al. fruit ripening, flies emerge from the puparium in the soil (2–15 cm in [2002 onward]). depth). Adult emergence tends to be synchronous, with most flies 2015 RODRIGUEZ-SAONA ET AL.: BLUEBERRY MAGGOT REVIEW 3

Fig. 5. Female R. mendax ovipositing in a mature blueberry, V. corymbosum, fruit.

Fig. 4. R. mendax pupa. likely a symbiotic relationship, where the bacteria provide the flies with nitrogen needed to fully mature their ovaries (Lauzon et al. 2000). Eggs require an incubation period of 3–10 d before hatching, (90%) emerging within a month’s period (Lathrop and Nickels depending on geographic locale and temperature (Lathrop and 1932, Lathrop 1952, Neunzig and Sorensen 1976). Females emerge McAlister 1931, Lathrop 1952, Neunzig and Sorensen 1976). Larvae 4–5 d before males, and their emergence coincides with maximal feed on the fruit pulp and complete development in the same fruit fruit availability (Bo¨ller and Prokopy 1976). Initial emergence and within which the egg was laid. Development under field conditions the rate of emergence for the population is dependent on soil tempera- takes between 17 and 30 d, depending on temperature; second instars ture, and has been modeled using degree-days (median emergence ¼ appear 8–9 d after egg hatching, while third instars appear 3–4 d later 934.3 degree-days, threshold ¼ 4.7C in New Jersey [Teixeira and last 6–9 d (Lathrop and Nickels 1932, Beckwith 1943, Lathrop and Polavarapu 2001a]; median emergence ¼ 971 degree-days, 1952, Neunzig and Sorensen 1976; Fig. 6). When larval development is threshold ¼ 6.1C in Maine [Dill et al. 2001]). In addition, in New complete, third instars drop to the soil, burrow, and pupate. Pupation Jersey, populations have been found to exhibit a delayed late summer commences in early July in the southern limit of its distribution and emergence (Teixeira and Polavarapu 2002, 2005a), possibly caused by may continue through to late September in the northern limit of its dis- a heat-induced quiescence at the pupal stage (Teixeira and Polavarapu tribution (Fig. 6). 2005b, c). Distribution and Host Plants. The blueberry maggot is a native fly Following emergence from the soil, flies mate and reproductively of North America (Payne and Berlocher 1995), and it is distributed in maturing females search for and imbibe food (7–10 d preoviposition the eastern United States as far south as Florida, Georgia, and Alabama, period; Smith and Prokopy 1981). Sexual maturation in females occurs and as far north and west as Maine, New Hampshire, Vermont, and when ovaries are fully developed (Prokopy and Papaj 1999). During Michigan (Geddes et al. 1987). In Canada, blueberry maggot was found and after reproductive maturation, males and females move to locations in Nova Scotia, Prince Edward Island, and New Brunswick between with ripe fruit. This is especially significant in lowbush blueberry, 1967 and 1988 (Guibord et al. 1985, Vincent and Lareau 1989). The where fields are usually managed on a 2-yr cropping cycle. Flies insect was first noted in southern Quebec in 1996 and in southern migrate from fields that are in the vegetative phase to fields that are Ontario in 1999 (CFIA 2012, Yee et al. 2013). Over the years, blueberry in the cropping or fruit production phase. Females lay eggs in predomi- maggot has steadily extended its geographical distribution in Quebec nantly ripe fruit (Fig. 5); normally, a single egg is placed in a single and Ontario (CFIA 2012). As of 2014, it has not reached the Lac noninfested fruit just under the fruit surface (Lathrop and McAlister St-Jean region, where most (85%) of Quebec’s managed lowbush 1931, Lathrop and Nickels 1932, Lathrop 1952). Many Rhagoletis spp. blueberries are produced without insecticide treatment (Ministe`re de females reportedly use oviposition marking pheromones to avoid l’Agriculture, des Peˆcheries et de l’Alimentation [MAPAQ] 2011a). competition among conspecifics (Nufio and Papaj 2001). Adults have a In addition to cultivated blueberry, blueberry maggot has been life span of 30–45þ d, and females can lay 25–100 eggs during their reported infesting a number of wild hosts. Hosts include lowbush blue- reproductive life (15–45 d, depending on temperature and other weather berry (V. angustifolium), sourtop blueberry [Vaccinium myrtilloides conditions; Lathrop and Nickels 1932, Lathrop 1952). Michx. (Kalm)], hillside blueberry (Vaccinium pallidum Ait.), highbush Olfactory cues are likely involved in adult blueberry maggot host blueberry (V. corymbosum), rabbiteye blueberry (Vaccinium ashei location. For instance, Averill et al. (1996) demonstrated that blueberry Reade), deerberry ( L.), lingonberry (Vaccinium maggot flies prefer its own berry host over hosts of other Rhagoletis vitis-idaea L.), black huckleberry (Gaylussacia baccata Wangenh.), species. Pelz-Stelinski et al. (2005) also captured more blueberry mag- dangleberry [Gaylussacia frondosa (L.) Torr. & A. Gray], and dwarf got flies on traps adjacent to host fruit. Liburd (2004) found attraction huckleberry [Gaylussacia dumosa (Andrews) Torr. & A. Gray] (Woods of blueberry maggot flies to butyl butanoate and cis-3-hexen-1-ol, two 1914, O’Kane 1914, Lathrop and Nickels 1931, Lathrop and Nickels host fruit volatiles. Interestingly, blueberry maggot flies are also 1932, Lathrop 1952, Smith et al. 2001, CFIA 2014). attracted to volatiles from Enterobacter (Pantoea) agglomerans,a Injury. Blueberry maggot is a direct fruit pest. Only feeding by the nitrogen-fixing bacteria living on the surface of leaves or fruit larvae results in fruit injury and there are no reports of injury solely due (MacCollom et al. 1992, 1994, 2009; Lauzon et al. 1998, 2000). This is to berry puncture during oviposition. Damage is generally unnoticeable 4 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 15, NO. 1

Fig. 6. Typical R. mendax life cycle in the northeastern United States and Canada (adapted from MAPAQ [2011b]). until larvae are in the third instar and much of the pulp has been con- sumed (Path and Woods 1922, Neunzig and Sorenson 1976). At this point, the berries loose turgidity, collapse, and shrivel (Fig. 7). The puparia are sensitive to desiccation so high-damage years tend to be those that have moderate levels of rainfall (Pearson and Meyer 1990). In addition, fields that are irrigated or have high weed densities that offer shade tend to be associated with higher levels of infestation (Dill et al. 2001). Flies are attracted to or reside longer in heavily weed- infested sections of fields, areas that have high fruit density, as well as in low spots in fields. Therefore, these areas tend to be associated with higher levels of fruit infestation. In lowbush blueberry, because of the 2-yr production cycle, the majority of flies invade fruit-bearing fields each year from field edges that support wild host plants or from nearby production fields that were in the fruit production cycle the previous year (Collins and Drummond 2004, Renkema et al. 2014). In this system, the flies enter the field and then appear to search randomly for suitable fruit for oviposition. On average, flies move 10 m per day in random direction. Similar results Fig. 7. Berry that lost its turgidity because of an attack by a have been found in highbush blueberries, where the population density R. mendax larva. of flies is high along field edges and decreases toward the field interior (C.R-S. and D.P., unpublished data). The resulting damage pattern due spherical traps (Fig. 9). These traps are baited with ammonium acetate to this behavior is an inverse relationship of infestation level and dis- to enhance attractiveness. Some extension specialists recommend tance into the field interior. deploying yellow panel traps early in the season and red spheres later in Larval infestation lowers the marketability of harvested fruit not only the season, when female flies are sexually mature. for fresh consumption but also for processing and exportation. There is Traps are used either to detect the presence of flies in the field on currently a zero-tolerance policy for fruit exported to Canada, which which insecticide applications are initiated (e.g. Wood et al. 1983, Gaul requires an intensive management program to avoid rejection for export et al. 1995), or used to estimate economic thresholds below which treat- (see section on Canadian Certification Program below for details). ment is not recommended (e.g. Dill et al. 2001, Gaul et al. 2002). In the United States, thresholds range from one fly per trap per week in high- Monitoring and Management bush blueberry (Rodriguez-Saona et al. 2010) to 10 flies per trap in low- Most research efforts in the past 30 yr have focused on the improve- bush blueberry (Dill et al. 2001). Traps are mainly placed on the field ment of monitoring for optimal timing with adulticides in commercial edge but are often combined with traps placed in the interior of fields. blueberry farms. Other efforts concerned alternatives to adulticidal Monitoring is used for determining general presence or for action treatments and postharvest management. thresholds in specific production areas. In the latter case, trap density Monitoring blueberry maggot flies is based upon the use of baited ranges from one trap per 4 ha in lowbush blueberry to one trap per 2 ha visual sticky traps: yellow flat panel traps (Fig. 8) or red or green in highbush blueberry. It is also recommended that traps be placed in 2015 RODRIGUEZ-SAONA ET AL.: BLUEBERRY MAGGOT REVIEW 5

Fig. 8. Yellow trap for monitoring R. mendax adults: placement in highbush blueberries and a close-up.

spheres (Fig. 9) than blue sphere (Liburd et al. 1998, Teixeira and Polavarapu 2001c). Liburd et al. (2000) captured more flies in traps 9 cm in diameter than 3.6- and 15.6-cm-diameter traps. There are advantages and disadvantages of using Pherocon-AM traps over the spheres. Because Pherocon-AM traps attract blueberry maggot immature flies looking for a food source, as opposed to fruit- type traps (spheres) that attract mature flies (Prokopy 1968, Neilson et al. 1984), they are more effective early in the season (Lathrop and Nickels 1932). For this reason, the spheres are less useful to determine the appropriate time of treatments. Pherocon-AM traps are, however, less effective at capturing blueberry maggot flies under low infestation levels and are also less target-specific than the spheres (Neilson et al. 1984). Compared with Pherocon-AM traps, spheres are more difficult to install and inspect (Neilson et al. 1984). Cultural Control. Cultural controls have a range of efficacies. Variety selection in highbush and rabbiteye blueberry offers potential to Fig. 9. Red sphere for monitoring R. mendax adults. reduce damage through the mechanism of “escape” by planting early maturing varieties. Whether this strategy offers a long-term solution in weedy sections of fields and in areas adjacent to abandoned fields or light of the variability in fly emergence time remains to be seen. natural areas that support wild host plants. The use of a harvesting machine to harvest all fruit left after hand Sticky Traps. Yellow sticky Pherocon-AM traps baited with ammo- harvesting is suggested as a means of eliminating late season oviposi- nium acetate to mimic a food source (Wood et al. 1983, Neilson et al. tion sites. It is also suggested that weed control may result in less favor- 1984) are most commonly used to monitor blueberry maggot adults. able habitat for fly survival in blueberry fields. An effective cultural These traps should be hung in a “V”orientation, with the yellow surface control for blueberry maggot fly in isolated lowbush blueberry fields is facing down (Fig. 8; Geddes et al. 1989; Teixeira and Polavarapu to manage entire fields on the same production cycle. Many growers 2001b, c). They should be placed within the top of the canopy for high- split fields so that half of the field is bearing fruit every year. However, bush blueberries (Teixeira and Polavarapu 2001c) or above plants for this results in a habitat where flies can move back and forth from emer- lowbush blueberries (Geddes et al. 1989), and at least 2 wk before first gence sites (vegetative sections) to fruit-bearing oviposition sites every flies are expected to emerge. Because ammonium acetate volatilize off year. Mulches (compost or pine needle) applied under highbush blue- the traps, they must be changed every 2 wk. Adding the symbiotic bac- berries after larvae drop from the berries have been shown to reduce teria E. agglomerans to monitoring traps increases the number of blue- emergence of flies from buried pupae, but this depends on soil moisture berry maggot fly captures in Pherocon-AM traps (MacCollom et al. and temperature (Renkema et al. 2011, 2012a). Another cultural control 2009). that may not be feasible for most growers is to produce blueberries in Sphere Traps. Liburd et al. (1998) found that blueberry maggot flies geographic areas in North America not yet inhabited by the blueberry are more attracted to spherical traps baited with ammonium acetate and maggot fly. protein hydrolysate than similarly baited Pherocon-AM traps. Similar Because lowbush blueberry is managed so that fruit is only pro- results were reported by Teixeira and Polavarapu (2001c) who also duced every other year (Yarborough 2009), isolated fields not within found differences in female sexual maturity captured in green plastic easy dispersal distance of blueberry maggot flies can avoid economi- spheres versus those captured in Pherocon-AM traps—green spheres cally damaging levels by managing the entire isolated field in one crop captured more immature females. Sphere color and size influence blue- cycle, i.e., either all fruit producing or all vegetative in a given year. berry maggot fly captures. Flies are more attracted to green and red This management tactic is strongly recommended (Yarborough and 6 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 15, NO. 1

Drummond 2014), and has been widely adopted in Maine (Rose et al. 2013). Chemical Control. In commercial situations, insecticide applications are currently the main tool for blueberry maggot management. Factors such as time to harvest, type of harvest (hand-picked or mechanical), market (fresh, frozen, or export), and reentry and preharvest intervals determine insecticide selection. Treatments are applied either as a pro- phylactic strategy or as an IPM strategy where treatments are based on economic thresholds. In both cases, monitoring population incidence or relative abundance forms the basis of decision-making. The most common application strategy in highbush blueberry is to treat the entire field or field sections if trap captures suggest control. Several strategies are used in lowbush blueberry. In Maine and Canada, treatment of emerging flies in adjacent vegetative phase fields is prac- ticed (Gaul et al. 2002, Drummond and Yarborough 2012, Renkema et al. 2014). In Maine, field perimeter applications are the norm (Collins and Drummond 2004). Deployment of traps in a grid and selective spot treatment adjacent to traps that exceed threshold levels is practiced in small fields. Perimeter insecticide treatments are practiced by many lowbush blueberry growers in Maine for blueberry maggot fly Fig. 10. Female D. alloeum ovipositing in a R. mendax-infested management (Rose et al. 2013). Traps are placed on the perimeter of blueberry fruit. the field with a few deployed in the field interior. When threshold levels are reached on traps in the field perimeter, insecticide treatments are applied in a 25–30-m perimeter band on the outside edge of the field Biological Control. Although biological control is not a recom- (Dill et al. 2001, Collins and Drummond 2004). mended option for blueberry maggot management in commercial blue- Although broad-spectrum insecticides (i.e., organophosphates and berry farms, there are several natural enemies known to attack the carbamates) are commonly used for blueberry maggot control larvae, pupae, and adults that can be conserved with the use of compati- (e.g. Oudemans et al. 2014), in the past decade, growers have increased ble control measures. While the fly is fairly cryptic, predation is known adoption of softer classes of insecticides, i.e., “reduced-risk” insecti- to occur by spiders (Lathrop and McAlister 1931). Larvae are parasi- cides, in particular those in the neonicotinoid class such as acetamiprid tized by braconids Opius melleus Gahan, Opius ferrugineus Gahan, (Assail) and imidacloprid. The target of insecticides applications is the and Diachasma alloeum Muesebeck (Fig. 10; Lathrop and McAlister adult fly; however, these neonicotinoids also have significant lethality 1931, Lathrop and Nickels 1932). Sharp and Polavarapu (1999) report on blueberry maggot larvae and eggs when applied topically to blue- an average of 10% larval parasitism by Diachasmimorpha (Opius) berry fruit postinfestation (Wise et al. 2014). The challenge for the mellea (Gahan) in New Jersey. The parasitoids apparently use fruit vol- future, in regards to blueberry maggot chemical control, is to maintain atiles for long-distance location of suitable hosts (Stelinski et al. 2004, a high level of control in a zero-tolerance market with reduced-risk 2006). For example, Stelinski et al. (2005) found that D. alloeum wasps insecticides that are often characterized by rapid environmental are attracted to volatiles from blueberry maggot-infested blueberry degradation. fruit. Larvae and pupae are attacked by ants (Formicidae; e.g., Formica There are also a few insecticide options for organic blueberry pro- fusca L. and Formica exsectoides Forel [Lathrop and McAlister 1931]) duction including spinosad (Entrust) and pyrethrum (PyGanic) insecti- and ground beetles (Carabidae; O’Neal et al. 2005; Renkema et al. cides (Barry et al. 2005, Drummond et al. 2008, Oudemans et al. 2014). 2012b, 2013). In general, however, predation and parasitism rates are The organically approved GF-120 Fruit Fly Bait, a baited formulation too low for effective suppression of blueberry maggot populations in of the insecticide spinosad, has also been effective in reducing blue- commercial blueberry farms (Bo¨ller and Prokopy 1976). Despite berry maggot infestation (Pelz et al. 2005, 2006; Rodriguez-Saona et al. attracting high numbers of ground beetles, Renkema et al. (2012) found 2008). that compost mulch does not lead to a reduction in numbers of blue- Behavioral Control. Sphere traps coated with an insecticide have berry maggot. Further research is needed on methods to augment and been used in research settings for controlling blueberry maggot flies in conserve these natural enemies in blueberry agro-ecosystems. an attract-and-kill strategy (Liburd et al.1999, 2003; Stelinski and Physical Control. Burning of blueberry plants is done for agronomic Liburd 2001; Stelinski et al. 2001; Barry et al. 2004; Barry and reasons, notably to rejuvenate the plants. Lathrop and Nickels (1932) Polavarapu 2005). Stelinski and Liburd (2001) found fewer blueberry burned hay as a combustible and, using emergence cages, they con- maggot larvae in blueberry fields treated with imidacloprid-coated cluded that burning has an indirect effect on blueberry maggot popula- spheres than untreated fields. Imidacloprid-treated spheres were more tions: blueberry maggot populations are depleted the year after because effective against blueberry maggot flies than spheres treated with other of very poor fruit set. neonicotinoid insecticides such as thiamethoxam and thiacloprid When sprayed, kaolin, a white, nonporous, fine-grained aluminosi- (Stelinski et al. 2001). Barry and Polavarapu (2005) also tested various licate mineral [Al4Si4O10(OH)8], commercialized as Surround WP, coating insecticides and found that fipronil and spinosad were the changes the color parameters (i.e., lightness, hue, and saturation) of most effective. Despite these efforts, attracticidal spheres have not been berries. In two-choice bioassays, females had a propensity (68%) to as effective in maintaining fields free of infestation as compared first visit the untreated blueberries (Lemoyne et al. 2008). Trials with with insecticidal sprays and are a more expensive control strategy, field-treated fruit showed that blueberries treated with Surround had which has limited their adoption. Although the use of insecticide- fewer oviposition scars than the control. This was more pronounced treated spheres appears to be promising in highbush blueberry, so with weekly applications of Surround. Surround also negatively far it has not been consistently effective in lowbush blueberry. Trapping affected oviposition by D. alloeum, a parasitoid of blueberry maggot out flies with sticky traps has not been shown to be effective in (Stelinski et al. 2006). lowbush blueberry, even at trap deployment distances of 3 m along field Postharvest Control. Dixon and Knowlton (1994) evaluated three edges. methods—brown sugar flotation technique, recovery trays, and fruit 2015 RODRIGUEZ-SAONA ET AL.: BLUEBERRY MAGGOT REVIEW 7 dissection—for detecting blueberry maggot larval infestation in fruit concentration of 3.5 kg per 20-litrer of water to 3 cm above the crushed postharvest, and recommended brown sugar flotation for rapid determi- berries. Larvae will float to the surface after shaking. nation. As often the case in postharvest situations, most research has According to the Directive D-02-04 (CFIA 2014), “if more than one focused on physical control methods (e.g., Hallman and Thomas 1999, larva is found in any one 2-L sample in the monitored production area, Hallman 2004). Gamma radiation can be used to treat blueberries after the fruit harvested that day may not be shipped to the fresh market in a harvest to kill all blueberry maggots present in fruit. For instance, Sharp non-regulated area. The fruit may, however, be sent to a processing and Polavarapu (1999) treated berries with 4-1200 Gy of gamma plant in a non-regulated area. These fruits may also be fumigated or fro- radiation and found that the treatment reduced the number of immature zen for 40 days prior to sale.” Furthermore, “if only one larva is found stages that pupated as well as the number of adults that emerged from in a 2-L sample, the fruit may be graded, either mechanically or by puparia. Similarly, Hallman and Thomas (1999) showed that 58 and hand-picking and sorting, re-sampled, and re-tested. If, upon re-testing, 24 Gy for apple maggot and blueberry maggot prevented 99% pupa- no larva is found, the blueberries may be shipped to the fresh market in tion, respectively, when irradiated as third instars in fruits. a non-regulated area. If the blueberries cannot be graded, as would be Prange and Lidster (1992) investigated the impact of an array of the case in ‘Pick-Your-Own’ establishments, the blueberries from that controlled atmosphere conditions (CO2 concentrations ranging from harvest for that monitored production area may not be sold on the fresh 0 to 100%, O2 at 2, 5, and 20%) at 5 or 21 C on the survival of blue- market.” berry maggot larvae, both exposed and in infested lowbush blueberry fruit. They found that optimal CO2 levels at 21 C reduced survivability Future Perspectives of blueberry maggot to 10%, while fresh fruit quality was not Pest management practices for blueberry maggot in blueberries adversely affected; however, this did not provide sufficient lethality to have dramatically changed over the past two decades. After the Food be useful to eliminate blueberry maggot larvae in fruit for quarantine Quality Protection Act was implemented in 1996 by the U.S. purposes. Environmental Protection Agency, several broad-spectrum insecticides Exposure of larvae and pupae at 20C for >2 d is lethal (Vincent have been under review, scheduled for cancellation, or severely et al. 2014). Reusable containers that origins from blueberry maggot- restricted for use in blueberries owing to potential surface water pollu- infested areas can be treated at 20C before being shipped to unin- tion, negative effects on wildlife, and worker exposure. As a result, fested areas. This method has been adopted by the Canadian Food research efforts were taken toward the evaluation, registration, and Inspection Agency Directive D-02-04 (CFIA 2014). increase grower adoption of new selective, reduced-risk materials. In Another method of postharvest control is to sort damaged fruit after the 2000s, a new class of insecticides, the neonicotinoids (i.e., acetami- harvest so that the sorted fruit is characterized by minimal or no prid and imidacloprid), became registered in blueberries. infestation. Peshlov et al. (2009) demonstrated that near-infrared spec- Neonicotinoids showed good efficacy against blueberry maggot, com- trometers could separate infested from noninfested blueberries in the parable with the standard broad-spectrum insecticides like phosmet. processing line, although the accuracy was 85–90%. Small incremen- Although many growers increased adoption of these new products, tal improvement of detection level might enhance damage sorting in others were reluctant to use neonicotinoids because of their potential processing facilities. negative effects on pollinators (Decourtye and Devillers 2010). Canadian Certification Program. To prevent further advances of Concurrently, research efforts were being made to decrease the amount blueberry maggot in uninfested areas, the CFIA enforces Directive of insecticides applied to control this fly. Because most flies invade D-02-04 (CFIA 2014). Accordingly, growers in infested areas that wish commercial blueberry fields from adjacent wild habitats or abandoned to ship blueberries to noninfested areas need to follow a series of moni- fields (Collins and Drummond 2004, C.R-S. and D.P., unpublished toring and control guidelines for blueberry maggot. For example, data), management efforts need to be targeted to fields near these areas. Directive D-02-04 applies to growers that wish to export blueberries Site-specific insecticide applications, where insecticides are applied from the United States to Canada, and for Canadian growers that ship only to specific fields with high risk of infestation, and border sprays, blueberries from an infested (e.g., Nova Scotia) to noninfested where insecticides are applied only to the first few rows along the edges (e.g., Quebec) areas. Growers have the option of either selecting an of a high-risk field, are two management methods that were evaluated IPM program, which involves placement of traps and the application of in Maine and New Jersey, and had become implemented in many registered insecticides when needed, or a calendar spray program, grower farms by the late 2000s. which involves applications of insecticides every 7–10 d beginning Growers were encouraged to use IPM-based programs. These 10 d after the first adult is captured in the region. Monitoring under the included: 1) monitoring for blueberry maggot populations using IPM program is done by the grower, while the state or local government Pherocon-AM traps, particularly in areas with high risk of infestation, monitors for the calendar spray program. The unit for monitoring is the i.e., along field edges near wooded areas; 2) targeting insecticide appli- “monitored production area” and Pherocon-AM traps are the standard cation only to fields where blueberry maggot flies are present; and 3) method for trapping. Trap density depends of the monitored production use of reduced-risk products if an insecticide application was needed. area and varies from 5 for 2 ha to >100 for >40 ha. New technologies such as Geographic Information Systems aided the In addition, the state or local government or its designee (usually the identification of high-risk areas within farms (Dobesberger and grower) takes samples from each monitored production area to ensure Macdonald 1993, C.R-S. and D.P., unpublished data). Growers started that the harvested fruit is free from blueberry maggot larvae. A mini- to see the results of these efforts in that IPM-based programs for blue- mum of one 2-liter sample of blueberries must be randomly taken for berry maggot were effective in maintaining fruit free from infestation each harvest from each monitored production area. The samples are and lowered insecticide cost and the number of applications per year. subjected to a hot water or sugar test. These methods are not used for These IPM-based programs were also expected to be compatible with purposes other than quality control and quarantine because they provide biological control and help conserve natural enemies of blueberry mag- information only after damage has occurred. The hot water test consists got and other pests. of placing the berries in a pot, covering them with water, and boiling Recent Pest Status. Throughout the 20th century, blueberry maggot them for at least 1 min. Berries are then emptied into a screen placed has been the major driver of entomological programs in blueberry. In over a pan with a black bottom, and gently crushed and rinsed with cold 2008, spotted wing drosophila, D. suzukii (Fig. 11), a new invasive pest water. The larvae can then be seen in the water against the dark back- of small fruit crops, was introduced into the U.S. mainland and has ground of the pan. The sugar test consists of placing the berries in a quickly spread throughout all major states where blueberries are pro- 4-liter container, gently crushing the berries, and then adding sugar at a duced (Hauser 2011, Walsh et al. 2011, Burrack et al. 2012). It was first 8 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 15, NO. 1

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(http://www.inspection.gc.ca/plants/plant-protection/ Beers 2012, Van Timmeren and Isaacs 2013)—to an entire farm earlier in directives/risk-management/rmd-11-03/eng/1330812746504/13308128493 the season, and continue with weekly applications until harvest. 76) (accessed 4 December 2014). Moreover, some of the insecticides that are effective against blueberry (CFIA) Canadian Food Inspection Agency. 2014. D-02-04: Phytosanitary maggot, like the neonicotinoids, are weak against spotted wing droso- requirements for the importation from the continental United States and for phila (Bruck et al. 2011), which has resulted in a decrease in use of neoni- domestic movement of commodities regulated for blueberry maggot, 5th Revision. Effective date: 21 June 2014. (http://www.inspection.gc.ca/plants/ cotinoid insecticides and an increase in broad-spectrum insecticide plant-protection/directives/horticulture/d-02-04/eng/1320046578973/ applications (D.P., unpublished data). 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