Blueberry IPM: Past Successes and Future Challenges

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Annual Review of Entomology Blueberry IPM: Past Successes and Future Challenges

Cesar Rodriguez-Saona,1,∗ Charles Vincent,2 and Rufus Isaacs3

1Department of Entomology, Rutgers University, New Brunswick, New Jersey 08901, USA; email: [email protected] 2Saint-Jean-sur-Richelieu Research and Development Centre, Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu, Quebec J3B 3E6, Canada; email: [email protected] 3Department of Entomology, Michigan State University, East Lansing, Michigan 48824, USA; email: [email protected]

Annu. Rev. Entomol. 2019. 64:95–114 Keywords The Annual Review of Entomology is online at Vaccinium, blueberry pest management, globalization, invasive species, ento.annualreviews.org maximum residue limits, MRLs https://doi.org/10.1146/annurev-ento-011118- 112147 Abstract Copyright c Her Majesty the Queen in Right of Blueberry is a crop native to North America with expanding production and Canada, as represented by the Minister of Agriculture and Agri-Food Canada consumption worldwide. In the historical regions of production, integrated pest management (IPM) programs have been developed and provided effec- ∗Corresponding author tive control of key insect pests. These have integrated monitoring programs with physical, cultural, biological, behavioral, and chemical controls to meet the intense demands of consumers and modern food systems. Globalization of the blueberry industry has resulted in new pest-crop associations and the introduction of invasive pests into existing and new blueberry-growing areas. Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. Invasive pests—in particular spotted wing drosophila—have been highly disruptive to traditional IPM programs, resulting in increased use of insecticides and the potential to disrupt beneﬁcial insects. Moreover, regulatory agencies have reduced the number of broad-spectrum insecticides available to growers while facilitating registration and adoption of reduced-risk insecticides that have a narrower spectrum of activity. Despite these new tools, increasing international trade has constrained insecticide use because of maximum residue limits, which are often not standardized across countries. Great potential remains for biological, behavioral, cultural, and physical methods to contribute to blueberry IPM, and with more regions investing in blueberry research, we expect regionally relevant IPM programs to develop in the new production regions.

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INTRODUCTION The term blueberry refers to the small fruit of some species of Vaccinium (family Ericaceae) that are native to North America (135). These species include lowbush blueberry (V. angustifolium, V. boreale, V. myrtilloides, V. pallidum,andV. angustifolium × V. corymbosum), southern (V. darrowii) and northern (V. corymbosum) highbush blueberry, and rabbiteye blueberry (V. ashei). These are a food source for wildlife and for indigenous people (59), and they also play an important role in the social fabric of these communities (105). In 1911, a project to domesticate highbush blueberry was initiated between Elizabeth White, a horticulturist for a private company in New Jersey (United States), and Frederick Coville, who was the chief botanist of the United States Department of Agriculture (28). The resulting cultivars were the foundation of the modern blueberry industry, which is built on germplasm from those early selections (102). North America remains the major region of highbush and lowbush blueberry production, and this is reﬂected in the relevant entomological literature. As other regions expand their production, there are increasing reports of new pest management challenges in those countries. We review the published research related to insect pest management and highlight areas where future studies are needed to ensure the long-term sustainability of blueberry production.

Global Blueberry Production Lowbush blueberries are typically grown in semi-wild systems, using slash and burn techniques developed by indigenous peoples (1). They are harvested from wild populations across eastern North America and from regions of major commercial production in Maine, Nova Scotia, New Brunswick, Prince Edward Island, and Lac Saint-Jean in Quebec (58). This industry has expanded rapidly in North America throughout the last two decades (121) to meet increased demand for processed blueberries used in baked goods and yogurts, and for fresh and processed organic fruit (24). Highbush blueberry fruit are used fresh and are also frozen for use in processed foods. After the initial cultivation in New Jersey a century ago, this sector of the blueberry industry grew steadily in the East and Midwest regions of the United States. Production in the United States has doubled in the past decade, largely from extensive plantings in the Southeast and West regions (13), but recently this growth has slowed (Figure 1a). In concert with the expansion, there has been rapid growth of blueberry production in Chile, Argentina, Mexico, China, South Africa, and Spain. This has created opportunities to advance horticultural practices, increasing production efﬁciency and per-hectare yields, resulting in the development of new domestic and international

Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org markets for fresh and processed blueberries. These changes have brought blueberry into regions Access provided by CASA Institution Identity on 10/08/20. For personal use only. without most of the community of insects that have evolved with these Vaccinium species in eastern North America. As such, many new blueberry producers have enjoyed a growing situation relatively free of insect pests. However, globalization has also raised the risk of pest importation to new regions and phytosanitary measures have been implemented to limit pest spread (17). International movement of fruit also raises the importance of maximum residue limits (MRLs) that can signiﬁcantly inﬂuence which pesticides can be used and the countries to which berries can be exported (22; Supplemental Text 1). Of the different commercialized plant species, northern highbush blueberries dominate worldwide production in terms of cultivated surface (75% northern highbush, 10% southern highbush, and 15% rabbiteye), weight, and value, and their production continues to increase (Figure 1b). From current production areas and new plantings, almost a million metric tons of blueberries are predicted to be produced by 2021 (13), with most of that expansion in new production regions.

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Growing Static Declining Limited planting b

1,000 Over 904 kt by 2021 900 Asia and Pacific Southern Africa Over 813 kt by 2019 800 Mediterranean and Northern Africa 700 Europe 600 South America North America 500

400

300

Blueberry production (kt) 200

100 0 2005 2008 2010 2012 2014 2016 2018 2020 Year

Figure 1 Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org

Access provided by CASA Institution Identity on 10/08/20. For personal use only. (a) Regions of the world where blueberry production is static (yellow), declining (red), or expanding (green). (b) Historical trends and projected future highbush blueberry production [in kilotons (kt)], based on current planting trends. Figure provided by Cort Brazelton of the International Blueberry Organization and adapted with permission.

Overview of Blueberry Insect IPM Blueberry plants are relatively well defended against arthropod pests, and they tend to have limited pest complexes compared with other perennial fruit crops such as apples, citrus, and grapes. However, they are still at risk from feeding on all parts of the plant and from vectors of diseases. Among the 24 insect species or taxa attacking blueberry in North America, Marucci (74) reported that the blueberry maggot ﬂy (Rhagoletis mendax) was the most serious pest in New Jersey, Michigan, Maine (United States), and Eastern Canada, as it required treatment most years. Other insects such as cranberry fruitworm (Acrobasis vaccinii), cherry fruitworm (Grapholita packardi), and

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a 140 Total 120 Monitoring Cultural/physical control 100 Chemical control Biological control Behavioral control 80 Host-plant resistance 60

scientific articles 40 Number of published

0 1914– 1950– 1960– 1970– 1980– 1990– 2000– 2010– 1949 1959 1969 1979 1989 1999 2009 2017 Year b 70 1914–1949 60 1950–1959 1960–1969 50 1970–1979 1980–1989 40 1990–1999 2000–2009 30 2010–2017

10 Published scientific articles (%)

0 Monitoring Cultural/ Chemical Biological Behavioral Host-plant physical control control control resistance control

Pest management approach

Figure 2 (a) Number and (b) percent of scientiﬁc articles about blueberry entomology published by decade about different pest management approaches (Supplemental Text 3). Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only.

plum curculio (Conotrachelus nenuphar) were of concern but of lesser importance. Entomological research and integrated pest management (IPM) programs have evolved ever since to adjust to new pests and new management techniques (Figure 2a,b) (27); this information is currently delivered through several venues (Supplemental Text 2). Managers of blueberry farms focus their IPM programs on protecting crop plant health while also protecting berries. Consequently, insect management is focused on direct pests that infest berries, such as the blueberry maggot ﬂy (109) and, more recently, the spotted wing drosophila (Drosophila suzukii) (6), as well as on pathogen vectors such as aphids (50) and ci- cadellids. Aphids are vectors of blueberry scorch virus and blueberry shoestring virus (50), while leafhoppers vector a phytoplasma that causes stunt (74); these are important diseases of blueberries.

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Forces Driving IPM Programs As a high-value crop that is often sold to be eaten as fresh berries, fruit must meet exacting insect- free standards (132), so growers face expectations to implement highly effective pest control. As a result, there tends to be signiﬁcant investment in pest management in commercial blueberry farms, including scouting and monitoring, sprayers, pesticides, and various postharvest processing equipment to remove infested berries. This is less of a concern for pick-your-own farms and roadside stands, where a low level of infestation may be tolerated. Many of the newer regions of blueberry production have been spared from the insect pest challenges found in historical centers of blueberry domestication. However, the spread of invasive pests, adoption of blueberry production under high tunnels, and global trade have all required IPM programs to adapt. As they do, there should be greater attention to nonchemical approaches for insect management (2, 33, 44). Sustainability concerns, such as energy use (39), can also inﬂuence how farms are managed. While blueberry sustainability programs are not as advanced as those developed for viticulture (20), we expect growth in this area to address the demand from markets that support farm environmental stewardship.

Impacts of Globalization on Blueberry Insect IPM As blueberry production has expanded globally, breeding programs have been established in many countries, supplying the nurseries and growers with regionally adapted cultivars (68). Though insect resistance is not a high priority for these programs, the promise of marker-assisted breeding (81) suggests that such traits will be increasingly integrated into blueberry cultivar development. International trade in blueberries increasingly results in quarantine insects playing an important role in which markets can be accessed. Phytosanitary requirements for insects have been met by growers following specific protocols, such as that for the blueberry maggot fly in which growers implement calendar sprays or they use monitoring-based IPM in which fly captures on traps trigger use of insecticides (17, 109). These berries must also meet MRLs, which vary widely among countries (see the section titled Global Trade and Maximum Residue Levels and Supplemental Text 1).

Historical Review of Research on Blueberry IPM This review highlights how IPM systems have been implemented in major regions of blueberry production and the effective management techniques that have been developed for key insect pests. Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org

Access provided by CASA Institution Identity on 10/08/20. For personal use only. We review responses to the new interactions between blueberries and pest insects created both by movement of this crop to new regions and by movement of invasive insects. A bibliometric search of publications on blueberry insects from 1914 to 2017 (Supplemental Text 3) was used to determine the temporal patterns of key IPM components. Using these references as a foundation, we highlight selected successes and challenges in blueberry IPM.

BLUEBERRY INSECT IPM Brief History of Blueberry Entomological Research Literature There has been a steady increase in the number of scientiﬁc publications on blueberry IPM since the 1970s, associated with the expansion in blueberry production in North America and globally (Figure 2a). Of these publications, chemical control (36% of 410 studies) has

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Sharp-nosed a Thrips leafhoppersp Blueberry aphidsp Cranberry/ Blueberry cherry gall midge fruitworm

Japanese beetle Spottedtted wingwing drosophilahila Plum curculio

Cutworms

Blueberry maggot fly

Others

b Global

Canada Europe United States Asia

South Africa America New Zealand

OR NC FL WA

MI Others

United States ME NJ Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. Figure 3 Proportion of scientiﬁc publications about blueberry entomology topics published (a)byinsectspeciesand(b) by region where the research was conducted. US states: NJ = New Jersey, ME = Maine, MI = Michigan, NC = North Carolina, FL = Florida, OR = Oregon, WA = Washington.

been the most studied, followed by biological (26%) and cultural/physical (11%) controls (Figure 2b). Within these publications, the most commonly studied insect pests of blueberries were fruit-feeding insects and vectors of diseases, which account for more than 50% of all studies (Figure 3a). Three major fruit-feeding insect pests—the blueberry maggot ﬂy, spotted wing drosophila, and cranberry fruitworm—account for 41% of all studies. Also, insect vectors of diseases such as leafhoppers and aphids constitute 8% of all studies. Most of our current knowl- edge on blueberry IPM comes from studies conducted in the United States and Canada (90% of all publications) (Figure 3b). Within the United States, most of these publications (>80%) have

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been conducted in New Jersey, Maine, Michigan, North Carolina, and Florida, with most of the rest from Oregon and Washington (Figure 3b). Zero tolerance for infested fruit and very low tolerance for insect vectors of diseases have been key aspects of blueberry IPM since the crop was domesticated. This has limited development of economic thresholds and the expansion of organic production. More recently, registrations of new insecticide classes and increasing importance of MRLs for exportation have further complicated chemical pest management options (Supplemental Text 1). Other factors that may inﬂuence use of certain pest management practices in blueberries include the size of the production area (e.g., small versus large farm), the type of farm (conventional, pick-your-own, organic, processed, fresh, etc.), and the composition of the surrounding landscape. However, information is still limited on the importance of these factors on pest pressure and IPM in blueberries [but see the study by Whitehouse et al. (141)].

Monitoring Research toward development of trapping methods to monitor insect pests of blueberries began in the 1960s and has increased throughout the years (Figure 2a). Improvement of monitoring tools was assisted by advances in chemical ecology, in particular through the identification of semiochemical attractants. Early on, sticky yellow trap boards baited with protein hydrolysate or ammonium acetate were found to be attractive to blueberry maggot flies (36, 49, 65). Sex and aggregation pheromones were identified to monitor several important blueberry pests (38, 78). Studies using baited traps have provided insight into flight activity (29, 116), dispersal behavior (83, 142), and spatial distribution (40, 112) of blueberry insect pests. This information has facilitated development of degree-day models (126, 128) and economic thresholds and injury levels (45, 143), helping target the optimal timing for management inputs.

Cultural and Physical Control Research on these control methods followed some key changes in insecticide use (Figure 2a,b; Supplemental Text 4). They were an important tool for insect pest management in the early years of blueberry production, but interest declined after broad-spectrum insecticides became available. In the past 20 years, their use has increased owing to restrictions on insecticides and expansion of organic production. Burning lowbush blueberry fields every second or third year is a common practice to promote fruit production and can also control the blueberry maggot fly, stem gall wasp, and flea beetle (47, 77), but not all insect pests are negatively affected by burning (145). Soil amendments such as cover crops, mulches, and tillage; pruning; handpicking infested Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. fruit; and the removal of alternative hosts are also of increasing interest (Supplemental Text 4). Pruning old canes is recommended for managing scales and stemborers, handpicking infested fruit has long been recommended for cranberry fruitworm and leafroller control, and removal of alternative hosts reduces black vine weevil (Brachyrhinus sulcatus) populations (10, 70, 96). Tillage of row middles reduces Japanese beetle (Popillia japonica) larval densities (52, 125), and ground covers increase adult abundance (124). Likewise, mulches can reduce blueberry maggot fly emergence from buried pupae (100). Exclusion netting (19), sanitation (46), and edible coatings (123) were shown to limit spotted wing drosophila infestation.

Chemical Control Chemical control has been an important component of IPM since blueberries became domesticated, even before the advent of synthetic insecticides (Figure 2a). Over the years, there have

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been changes in insecticide use patterns as a result of environmental and public concerns leading to more regulatory restrictions. Also, research on blueberry IPM has shifted attention toward alternatives to chemical control (Figure 2b). Prior to 1950, inorganic insecticides such as lead arsenate were commonly evaluated for blueberry pest control (23, 27, 60, 61, 80). Botanical insecticides such as rotenone and nicotine were also tested at the time (11, 60); but they were often found to be less effective, less durable, and more expensive than inorganic insecticides. Starting in the mid-1940s, research on broad-spectrum insecticides such as DDT and parathion became common (75, 96, 129). Organophosphate (OP) and carbamate insecticides were studied in the 1960s, but at this time, awareness of environmental side effects of insecticides increased. Several studies have since documented the negative impacts on bees of insecticides applied to blueberries and neighboring habitats (41, 56, 76, 92, 122, 130, 146). DDT applied to lowbush blueberries had long-term negative effects on salmon populations in Maine (69). A significant change in insecticide use in US blueberries occurred after the implementation of the Food Quality Protection Act (131). Several broad-spectrum insecticides were eliminated (e.g., azinphos-methyl, endosulfan) or are under review. This prompted registration of new insecticides considered reduced-risk or OP alternatives owing to their lower mammalian toxic- ity, relative safety to the environment, and greater compatibility with IPM practices such as biological control. Many of these newer insecticides were adopted in blueberries (53). For example, neonicotinoid insecticides for control of blueberry maggot fly, aphids, Japanese beetle, and oriental beetle (Anomala orientalis); spinosyn insecticides for control of thrips; insect growth regulators for controlling cranberry fruitworm and plum curculio; and, more recently, the an- thranilic diamide insecticides for many pests but mainly Lepidoptera (96, 110, 113, 144). Dur- ing the 2000s, reduced-risk insecticides were used throughout blueberry-producing regions of North America. However, owing to their specificity, occasional pests such as bud mites and scales increased in abundance in some regions. To date, only a few effective insecticides are available for organic production (9). Kaolin clay has been tested for blueberry maggot fly, thrips, and aphids (63, 118), and spinosad for lepidopteran pests, blueberry maggot fly, and thrips (87). Spinosad has been adopted widely in organic blueberry production owing to its broad efficacy. In the last decade, spotted wing drosophila has become a major entomological driver of IPM programs. Relatively inexpensive broad-spectrum insecticides (OPs, carbamates, and pyrethroids) are effective against this pest (134), thus limiting implementation of reduced- risk chemistries and challenging progress toward broader IPM implementation. This invasive pest has created several challenges: Farmers need to spray more often (i.e., 7–10-day intervals) during harvest, rotate among insecticides from only five chemical classes to avoid de- Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. velopment of resistance, comply with MRLs for export to other countries (Supplemental Table 1), and select effective insecticides from a short list with very short (1-day) preharvest intervals (22, 134). Pollinator protection is important for blueberry production, with increasing significance due to concerns about declining honey bees and wild bees. Blueberry growers rely on bees for pollination (37) and must ensure that applications of insecticides do not harm bees. Timing applications to avoid pollinator exposure and using reduced-risk insecticides are important for bee conservation (130), but this can be challenging, particularly when controlling pests ac- tive during bloom. Avoiding spraying completely during bloom can avoid risk to bees, but many growers use Bacillus thuringiensis, Beauveria bassiana (149), or methoxyfenozide during bloom for control of lepidopteran and coleopteran pests and apply at night to minimize risk to pollinators.

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Biological Control Since the beginning of commercial blueberry production, identification of biological control agents attacking various insect pests has been of great interest (73, 84, 99) (Figure 2b). How- ever, implementation of strategies to enhance biological control has been limited. This reflects the intensity of pest management to meet market demands combined with challenges of cultural practices to promote natural enemies. Bacillus thuringiensis has long been used for lepidopteran pests, and this is highly compatible with natural enemies; however, its efficacy can be variable and may require multiple applications (96, 115). Relatively little is known about the impact of natural enemies on pest populations in commercial blueberry production. Jones et al. (55) reported higher predator activity based on removal of sentinel pupae in blueberry field interiors than at field edges. Natural enemies have a negative impact on thrips (24) as well as spotted wing drosophila pupae in both lowbush (7) and highbush (141) blueberries. Spiders can play an important role in pest suppression and are associated with lower strawberry rootworm and grasshopper populations (25, 72) and fewer thrips infestations (149). While biological control may not be sufficient to keep fruit from being damaged, it can work in combination with other tactics to maintain insect pests below economic thresholds. Cultural and chemical controls can have disruptive effects on natural enemies. For instance, pruning by burning can increase pest abundance in lowbush blueberries because of a lower abundance of ants and spiders (24), and insect predator and parasitoid populations are reduced by insecticide applications (18, 149). Whalon & Elsner (140) reported negative effects of insecticides on predators of the aphid Illinoia pepperi in blueberries. Treatment with kaolin clay particle film (Surround WP) disrupted host finding and oviposition by Diachasma alloeum,a blueberry maggot fly parasitoid (120). Changes in IPM practices due to stricter regulations on insecticides may allow for the adoption of strategies to conserve natural enemies. For example, abundance of the predatory ground beetle Harpalus erraticus (85) and aphid parasitism (51) were higher in insect control programs that implemented reduced-risk insecticides compared with those based on broad-spectrum insecticides. Abundance of harvestman (Opiliones) (26) and ladybird beetles (136) was higher in organic than in conventionally managed blueberry fields (26). Habitat manipulation has been evaluated recently in blueberries for enhancing biological control. Walton & Isaacs (139) and Blaauw & Isaacs (12) showed that wildflower strips can increase natural enemy abundance in adjacent highbush blueberry fields and can enhance biological control. Ganter et al. (34) and Renkema et al. (101) found both positive and negative effects on the abundance of predatory beetles in blueberry soils on the basis of the type of mulch. Because most blueberry pests are native to North America, where most research has been Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. done (Figure 3b), relatively little attention has been paid to foreign exploration to find natural enemies. Horgan et al. (48) evaluated the effects of the introduced parasitoid Cyzenis albicans on winter moth, Operophtera brumata, in birch woodlands and blueberries and found high levels of parasitism in outbreak years. Foreign exploration is underway for spotted wing drosophila parasitoids (21). Augmentative biological control of insect predators, parasitoids, and pathogens has also been evaluated for a few pest species of blueberries but has yet to be widely adopted for their control. Releases of predators of flower thrips have been evaluated in blueberry fields with inconclusive results (5). Inundative releases of the egg parasitoid Trichogramma minutum for oblique-banded leafroller (Choristoneura rosaceana) control (79) and of the entomopathogenic nematode Steinernema scarabaei for control of white grubs (91) have also been evaluated. The entomopathogenic fungus Beauveria bassiana reduced citrus thrips in blueberries and could provide useful control in organic production (150).

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Host-Plant Resistance Breeding for insect-resistant blueberry cultivars has been a relatively low priority, given the demand for cultivars with improved fruit quality and quantity. Therefore, host-plant resistance has been under investigation only in the last 20 years (Figure 2a,b). A few studies have identified insect-resistant cultivars, with fewer studies on the mechanisms involved in this resistance. Vac- cinium ashei was more resistant to sharp-nosed leafhoppers (Scaphytopius magdalensis) compared to V. corymbosum (29). In contrast, V. ashei cultivars were more susceptible to the Nearctic gall midge, Prodiplosis vaccinia, than southern highbush blueberry cultivars (15). Differences in oviposition preference were observed for the stem borer, Oberea myops, among V. ashei cultivars (147). Van Timmeren & Isaacs (133) also reported differential resistance of V. corymbosum cultivars to two fruit and foliar insect pests: the cranberry fruitworm and Japanese beetle. Ranger et al. (98) showed higher resistance to blueberry aphid, I. pepperi, in wild Vaccinium spp. compared to cultivated highbush blueberries, and the abundance of various tephritid fruit flies (31), thrips (103), and glassy-winged sharpshooter adults (127) also varied among southern highbush varieties (V. corymbosum × V. darrowi). The application of genomic techniques to breeding programs (81) is poised to bring much greater understanding of the genetic basis and mechanisms of resistance, which should translate into greater pest resistance combined with desirable horticultural traits. Host-plant phenology can greatly affect insect pest damage in blueberries. Early-ripening highbush blueberry cultivars had lower larval infestation by blueberry maggot fly than later- maturing cultivars (65). Similarly, early-ripening highbush cultivars may escape infestation by spotted wing drosophila (44). In contrast, plum curculio oviposition scars were more abundant on early- and mid-season highbush blueberry cultivars than on late-season cultivars (89). Physical traits are also important. Spotted wing drosophila lays more eggs in softer than in firmer fruits, and oviposition increases as penetration force decreases (57, 62). Spraying fruit with calcium silicate increased penetration force and firmness and reduced eggs laid by spotted wing drosophila (62). Blueberries contain a variety of defensive compounds, mainly phenolics, which can provide resistance against insect pests. However, not all insects are equally affected. Higher content of phenolic acids, flavonoids, and tannins in leaves of highbush blueberries correlated with lower numbers of leafroller larvae (35). Total phenolics in Vaccinium spp., however, did not correlate with aphid resistance (98). Lee et al. (62) showed that oviposition by spotted wing drosophila increases with increasing pH and brix (total soluble solids) in fruit. In contrast, Little et al. (67) reported higher spotted wing drosophila preference for fruits with lower brix and lower pH levels. Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. Behavioral Control Only in the past 20 years have behavioral control strategies been researched for managing blueberry pests (Figure 2a,b). These strategies are particularly appealing for organic blueberry production because they can be based on natural products and can reduce insecticide applications. Insecticide- impregnated spheres (94, 95, 148) have been evaluated as an attract-and-kill strategy for controlling the blueberry maggot fly. Neonicotinoid (e.g., imidacloprid)-treated spheres increase fly mortality under laboratory and field conditions and reduce fruit infestation in the field, and adding a feeding stimulant (sucrose) enhances their effectiveness (66, 119). However, owing to the relatively high cost of the spheres and lack of interest from manufacturers, currently they are not available commercially to farmers. GF-120 Naturalyte Fruit Fly bait, a commercial product containing an insecticide (spinosad), sugar, and attractants, suppresses blueberry maggot fly populations and is available for organic production (9, 87).

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Mating disruption for oriental beetle is a good example of a technology that was developed by university researchers and is now a commercial product used by blueberry farmers in the United States. Three formulations have been evaluated: a microencapsulated sprayable formulation (90), point-source dispensers (bubbles) (113), and a sprayable Specialized Pheromone and Lure Appli- cation Technology (SPLAT) formulation (108). Dramatic reductions in adult beetle populations and larval infestation have been documented for all three formulations. Because the oriental beetle sex pheromone is a ketone, it does not have tolerance exemption in fruit crops due to potential food contamination, so only the hand-applied dispensers are commercialized. More recent research has focused on behavioral control tactics for spotted wing drosophila. Mass trapping has been attempted with mixed results (44, 93). This tactic could be used in small production areas or tunnel production systems but might not be economical for large farms or where there is high pest pressure and zero tolerance for infested fruit. A shortcoming of mass trapping for spotted wing drosophila is that traps are currently not efficient at capturing a high per- centage of flies (44). Placing traps outside blueberry fields or using attractants in combination with insecticides have been suggested as alternative attract-and-kill scenarios (44). Yeast has also been evaluated as an attractant for spotted wing drosophila (82), and insecticide-impregnated spheres developed for Rhagoletis spp. can be effective at attracting and killing the adults (104). The potential of combining an attractant (as a pull component) with a repellent (as a push component) in a push-pull system for spotted wing drosophila is being explored (138). Further studies are needed to investi- gate the conditions under which these behavioral control strategies are economically viable such as farm size, surrounding landscape composition, pest pressure, and other management practices.

Postharvest Control In 2016, 35.5% of the total North American crop (by weight) was sold as fresh blueberries, while 64.9% was sold for processing (13). Entomological standards for berries (e.g., presence of larvae in fruit) are generally the same for both markets (132). However, when growers consider exporting berries, they have to comply with the regulations of importing countries, not only to satisfy consumers but also to avoid disseminating insects into non-infested areas. For example, fresh, frozen, and dried blueberries exported from Canada to Japan require a phytosanitary certificate from the Canadian Food Inspection Agency (CFIA) and are subject to inspection by Japanese authorities (16). Constraints also exist for movements of berries within countries. Thus the CFIA requires treatment of empty, reusable berry containers to prevent dissemination of the blueberry maggot fly from infested to non-infested areas of Canada (17). Postharvest treatments are frequently required by importing countries to avoid undesirable Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. insect species. Chemical and physical methods have been used extensively for postharvest control of blueberry pests. For instance, fumigants such as carbon bisulphide, ethylene oxide, methyl bromide, and ethylene dibromide were tested in the early years of blueberry production to control Japanese beetle, cranberry fruitworm, plum curculio, and blueberry maggot fly infestation in harvested blueberries (10, 86, 111). The blueberry maggot fly can be detected on the processing line using near infrared spectroscopy; however, because the accuracy is only 80% (88) it has not been adopted. Physical control methods such as cold storage have been tested more recently. Jessup et al. (54) showed no survival of tephritid larvae (Batrocera tryoni) infesting rabbiteye blueberries when stored at 1◦C for 12 days. Exposing larvae in berries and pupae to cold temperatures (−20◦C) for >2 days prevented blueberry maggot adult emergence (137). When spotted wing drosophila– infested blueberry fruit was stored at <2◦C for 72 h, no eggs survived to pupation, larval development was prolonged, and larval survival was reduced by 41% (3). Although irradiation quarantine

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treatments have also been evaluated to prevent pupation and adult emergence of blueberry maggot ﬂies (43, 114) and oviposition by plum curculio (42), this method has yet to be employed at a commercial scale.

IMPACT OF GLOBALIZATION ON BLUEBERRY IPM

Challenges for Sustainable IPM Since blueberries are perceived as healthy fruit by the public, the blueberry industry supports health research and marketing to maintain this positive perception. Historically, blueberry growers enjoyed a relatively easy situation in terms of entomological challenges likely owing to mostly native pests and a native host plant that have provided some reciprocal coevolutionary balance. Wher- ever it occurred, the blueberry maggot ﬂy was the main insect pest managed using science-based IPM programs across eastern North America (109). With the arrival of spotted wing drosophila across most global regions of blueberry production, this has become the major insect pest concern, putting great strain on the design and economics of IPM programs for blueberry and other berry crops throughout the world.

Invasive Pests and Insect Pests Threatening Blueberry Production Globally Invasive pests are non-natives with a propensity to spread and cause economic losses. Spotted wing drosophila is a clear example, but additionally, the brown marmorated stink bug, Halyomorpha halys, was ﬁrst collected in North America (Pennsylvania) in 1996 and its range and crop impacts have expanded to major agricultural regions (64). Blueberry is one of its hosts (143), but so far it is not a major concern for the blueberry industry. Wherever spotted wing drosophila coexists with cultivated blueberry plants, it will likely be the main insect challenge, at least in the near future. Spotted wing drosophila attacks fruit throughout the ripening season, requiring intensive management to achieve zero infestation. This pest is now distributed globally (4, 6; Supplemental Text 5). As discussed previously, the global area of blueberry farms is increasing dramatically (Figure 1a,b). Within these new production areas, the entomological challenges will be of two kinds: either from the native pests found in new production areas or from exotic or introduced pests. The native pests will also be regional in nature, as highlighted by Rocca & Greco (106), who studied the richness and diversity of herbivorous insects associated with highbush blueberry farms near Buenos Aires and Entre Rıos´ (Argentina), where highbush blueberries were introduced in the Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. 1990s as a crop for export. They produced a list of 37 insect species belonging to 31 families, most being hemipterans (51.6%), followed by lepidopterans (19.3%), coleopterans (16.5%), and or- thopterans (6.6%), while hymenopterans and thysanopterans were <3.2%. Aphidae was the most abundant family in all sites, followed by different families, depending on surrounding crops and their associated herbivores. The richness and diversity of species varied among phenological stages and years. Rocca & Greco (107) developed presence-absence sampling plans for aphids that reach high densities (Aphis gossypii and A. spriraecola) based on sampling blueberry ﬁelds around Buenos Aires.

Global Trade and Maximum Residue Levels Blueberries are a global crop being grown in approximately 30 countries (Figure 1a). As the industry has expanded, there has been an associated increase in transportation of fruit from major

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regions of production to areas where fruit can be marketed, with approximately 25% of all blueberries being exported (30). Such international trade increases the risk of nonnative pests being introduced, as exemplified by the rapid spread and complex invasion routes taken by spotted wing drosophila around the world in the past five years (32). As mentioned above, pesticide residues become very important for fresh and processed fruit transported across international borders. This is because each importing country sets a limit for each specific pesticide residue on food crops (71), and these MRLs can vary by orders of magnitude among different countries (Supplemental Text 1). These MRLs are increasingly important for the selection of pesticides and timing of harvest by growers, as well as the decisions that marketers make to direct their fruit to different export markets. To help access these export markets, producers are designating specific fields for particular countries and designing an IPM program with particular pesticides that can meet their MRLs. These decisions are being supported by two complementary lines of research. The first studies pesticide residue declines using in-field applications and analysis of residues on fruit collected at different times after application, while the other approach samples fruit from farms at harvest time to determine how typical or new spray programs relate to the levels of residue present in berries (Supplemental Text 1). For example, Diepenbrock et al. (22) used the latter approach in North Carolina and Georgia and found rotational insecticide programs that can reduce infestation from spotted wing drosophila while also allowing growers to meet export MRL requirements.

FUTURE CHALLENGES FOR BLUEBERRY INSECT IPM There are challenges for sustainable IPM programs in traditional and new areas of blueberry production. In the traditional areas, much of the research on blueberry insects has been focused on direct fruit-feeding pests and, to a lesser extent, on insect vectors of diseases such as aphids and leafhoppers (Figure 3a). For example, the sharp-nosed leafhopper, a vector that transmits a phytoplasma that causes blueberry stunt, poses an important threat to New Jersey blueberries, where it is the only regular target for postharvest sprays. Further research on insect/disease/blueberry interactions will be required in traditional and new areas where blueberries are grown. In areas where blueberries are nonnative, it is likely that new arthropod complexes will become pests. As an example, spotted wing drosophila was thought to be detected in Chile in 2016 (Supplemental Text 5) but taxonomic expertise proved otherwise. More recently, it has been determined that this insect does occur in Chile, triggering management responses by the govern- ment and growers. In these areas, much research will be needed to quickly develop science-based and regionally relevant IPM programs. Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. One research area that has been overlooked is the management of blueberry fields at the landscape level. For example, Smith et al. (117) demonstrated that, in Michigan, wild plant species (e.g., Gaylussacia baccata and G. dumosa) are hosts of blueberry maggot fly and therefore may act as reservoirs of this pest. Ballman & Drummond (8) found a correlation between fruit infestation by spotted wing drosophila from surrounding woodland alternative hosts and adult fly densities in nearby commercial blueberry fields. These findings indicate that special care must be taken in implementing monitoring programs that will help determine risks caused by insect pests at landscape levels. Advances in molecular diagnostics can prove to be useful in some situations, notably to assess the success of IPM programs or to demonstrate compliance with export standards. Until recently, it was difficult for nontaxonomists to identify larvae inside fruit. It is now possible to identify the blueberry maggot fly with real-time polymerase chain reaction (14). The state of molecular biology is such that development of diagnostic tests is fast, reliable, and affordable; however,

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the sensitivity might result in increased pressure to apply insecticides to eliminate very small likelihoods of infestation. Finally, as consumer demand for organic blueberries increases worldwide, there is a need for management tactics that comply with organic labels. In that market segment, much research has been done since the 1980s (Figure 2a) in North America, but sustained research and extension (Supplemental Text 2) efforts are required, notably for effective non-insecticidal (and non- pesticidal) tactics, to maintain sustainable IPM programs.

DISCLOSURE STATEMENT The authors are not aware of any afﬁliation, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS The authors thank the International Blueberry Organization for their permission to use the information in Figure 1, and Cort Brazelton for his insights into recent planting trends. We thank Robert Holdcraft for excellent assistance with graphics, and Frank Drummond, Dean Polk, and anonymous reviewers for their feedback on draft versions. We thank Michelle Bargel (senior information specialist, Canadian Agriculture Library, London, Ontario) for searching and com- piling the list of publications used to prepare this article. C.R.-S. and R.I. were supported by the USDA-NIFA Specialty Crops Research Initiative (2015-51181-24252), C.R.-S. by the Hatch project (NJ08140), and C.V. by the NOI A-Base program of Agriculture and Agri-Food Canada.

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56. Kevan PG, Greco CF, Belaoussoff S. 1997. Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystemic health: pesticide stress on pollinators on blueberry heaths. J. Appl. Ecol. 34:1122–36 57. Kinjo H, Kunimi Y, Ban T, Nakai M. 2013. Oviposition efﬁcacy of Drosophila suzukii (Diptera: Drosophil- idae) on different cultivars of blueberry. J. Econ. Entomol. 106:1767–71 58. Kinsman GB. 1993. The History of Lowbush Blueberry Industry in Nova Scotia 1950–1990. Truro: Nova Scotia Dep. Agric. Mark. 59. Kuhnlein HV, Turner NJ. 1991. Traditional Plant Foods of Canadian Indigenous Peoples: Nutrition, Botany, and Use. Amsterdam, Neth.: Gordon and Breach 60. Lathrop FH. 1939. Ten years of warfare against the blueberry maggot. J. Econ. Entomol. 32:510–13 61. Leach BR, Fleming WE, Johnson JP. 1924. Soil insecticide investigations at the Japanese beetle laboratory during 1923. J. Econ. Entomol. 17:361–65 62. Lee JC, Dalton DT, Swoboda-Bhattarai KA, Bruck DJ, Burrack HJ, et al. 2016. Characterization and manipulation of fruit susceptibility to Drosophila suzukii. J. Pest Sci. 89:771–80 63. Lemoyne P, Vincent C, Gaul S, Mackenzie K. 2008. Kaolin affects blueberry maggot behavior on fruit. J. Econ. Entomol. 101:118–25 64. Leskey TC, Nielsen AL. 2018. Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management. Annu. Rev. Entomol. 63:599–618 65. Liburd OE, Alm SR, Casagrande RA. 1998. Susceptibility of highbush blueberry cultivars to larval infestation by Rhagoletis mendax (Diptera: Tephritidae). Environ. Entomol. 27:817–21 66. Liburd OE, Gut LJ, Stelinski LL, Whalon ME, McGuire MR, et al. 1999. Mortality of Rhagoletis species encountering pesticide-treated spheres (Diptera: Tephritidae). J. Econ. Entomol. 92:1151–56 67. Little CM, Chapman TW, Moreau DL, Hillier NK. 2017. Susceptibility of selected boreal fruits and berries to the invasive pest Drosophila suzukii (Diptera: Drosophilidae). Pest Manag. Sci. 73:160–66 68. Lobos GA, Hancock JF. 2015. Breeding blueberries for a changing global environment: a review. Front. Plant Sci. 6:782 69. Locke DO, Havey K. 1972. Effects of DDT upon salmon from Schoodic Lake, Maine. Trans. Am. Fish Soc. 101:638–43 70. MacKenzie K, Hayman D, Reekie E. 2004. The effect of pruning on blueberry stem gall wasp. Small Fruits Rev. 3:331–38 71. MacLachlan DJ, Hamilton D. 2010. Estimation methods for Maximum Residue Limits for pesticides. Regul. Toxicol. Pharmacol. 58:208–18 72. Maloney DM, Alford AR, Drummond FA. 2005. Predation by Lycosidae in lowbush blueberry agroe- cosystems. Trends Entomol. 4:43–57 73. Mampe CD, Neunzig HH. 1967. The biology, parasitism, and population sampling of the plum curculio on blueberry in North Carolina. J. Econ. Entomol. 60:807–12 74. Marucci PE. 1966. Insects and their control. In Blueberry Culture, ed. P Eck, NF Childers, pp. 199–235. New Brunswick, NJ: Rutgers Univ. Press Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. 75. Maxwell CW. 1961. Field tests of insecticides against the thrips Frankliniella vaccinii Morgan and Tae- niothrips vaccinophilus Hood on the low-bush blueberry. Can. J. Plant Sci. 41:134–36 76. Mayer DF, Johansen CA, Shanks CH Jr., Antonelli AL. 1989. Methomyl insecticide and domesticated pollinators. J. Entomol. Soc. B. C. 86:7–13 77. McAlister LC, Anderson WH. 1932. The blueberry stem-gall in Maine. J. Econ. Entomol. 25:1165–69 78. McDonough LM, Averill AL, Davis HG, Smithhisler CL, Murray DA, et al. 1994. Sex pheromone of cranberry fruitworm, Acrobasis vaccinii (Lepidoptera: Pyralidae). J. Chem. Ecol. 20:3269–79 79. McGregor R, Caddick G, Henderson D. 2000. Egg loads and egg masses: parasitism of Choristoneura rosaceana eggs by Trichogramma minutum after inundative release in a commercial blueberry ﬁeld. Bio- Control 45:257–68 80. Metzger FW, Lipp JW. 1936. Value of lime and aluminum sulfate as a repellent spray for Japanese beetle. J. Econ. Entomol. 29:343–47 81. Moose SP, Mumm RH. 2008. Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol. 147:969–77

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82. Mori BA, Whitener AB, Leinweber Y, Revadi S, Beers EH, et al. 2017. Enhanced yeast feeding following mating facilitates control of the invasive fruit pest Drosophila suzukii. J. Appl. Ecol. 54:170–77 83. Morimoto KM, Ramsdell DC. 1985. Aphid vector population dynamics and movement relative to field transmission of blueberry shoestring virus. Phytopathology 75:1217–22 84. Nickle WR, Wood GW. 1964. Hojvardula aptini (Sharga 1932) parasitic in blueberry thrips in New Brunswick. Can. J. Zool. 42:843–46 85. O’Neal ME, Mason KS, Isaacs R. 2005. Seasonal abundance of ground beetles in highbush blueberry (Vaccinium corymbosum) fields and response to a reduced-risk insecticide program. Environ. Entomol. 34:378–84 86. Osburn MR. 1931. Effect on certain fresh fruits of fumigation with ethylene oxide to destroy the Japanese beetle. J. N. Y. Entomol. Soc. 39:567–75 87. Pelz KS, Isaacs R, Wise JC, Gut LJ. 2005. Protection of fruit against infestation by apple maggot and blueberry maggot (Diptera: Tephritidae) using compounds containing spinosad. J. Econ. Entomol. 98:432–37 88. Peshlov BN, Dowelt FE, Drummond FA, Donahue DW. 2009. Comparison of three near infrared spectrophotometers for infestation detection in wild blueberries using multivariate calibration models. J. Near Infrared Spectrosc. 17:203–12 89. Polavarapu S, Kyryczenko-Roth V, Barry JD. 2004. Phenology and infestation patterns of plum curculio (Coleoptera: Curculionidae) on four highbush blueberry cultivars. J. Econ. Entomol. 97:1899–905 90. Polavarapu S, Wicki M, Vogel K, Lonergan G, Nielsen K. 2002. Disruption of sexual communication of oriental beetles (Coleoptera: Scarabaeidae) with a microencapsulated formulation of sex pheromone components in blueberries and ornamental nurseries. Environ. Entomol. 31:1268–75 91. Polavarapu SK, Koppenhofer¨ AM, Barry JD, Holdcraft RJ, Fuzy EM. 2007. Entomopathogenic nem- atodes and neonicotinoids for remedial control of oriental beetle, Anomala orientalis (Coleoptera: Scarabaeidae), in highbush blueberry. Crop Prot. 26:1266–71 92. Pritts MP. 1997. Impacts of cultivation practices on pollination of Vaccinium. Acta Hortic. 446:91–96 93. Profaizer D, Grassi A, Zadra E, Maistri S. 2015. Efficacy of insecticide treatment strategies against Drosophila suzukii in combination with mass trapping. IOBC/WPRS Bull. 109:215–18 94. Prokopy RJ, Wright SE, Black JL, Hu XP, McGuire MR. 2000. Attracticidal spheres for controlling apple maggot flies: commercial-orchard trials. Entomol. Ex. Appl. 97:293–99 95. Prokopy RJ, Wright SE, Chandler B, Hu XP. 1998. Evaluation of varying doses of different toxicants for use on spheres to control apple maggot flies. Fruit Notes 63:6–11 96. Raine J. 1965. Control of Dasystoma salicellum, a new pest of blueberries in British Columbia. Can. J. Plant Sci. 45:243–45 97. Ramanaidu K, Hardman JM, Percival DC, Cutler GC. 2011. Laboratory and field susceptibility of blueberry spanworm (Lepidoptera: Geometridae) to conventional and reduced-risk insecticides. Crop Prot. 30:1643–48 Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. 98. Ranger CM, Johnson-Cicalese J, Polavarapu S, Vorsa N. 2006. Evaluation of Vaccinium spp. for Illinoia pepperi (Hemiptera: Aphididae) performance and phenolic content. J. Econ. Entomol. 99:1474–82 99. Renkema JM, Cutler GC, Rutherford K. 2014. Molecular analysis reveals lowbush blueberry pest predation rates depend on ground beetle (Coleoptera: Carabidae) species and pest density. BioControl 59:749–60 100. Renkema JM, Lynch DH, Cutler GC, MacKenzie K, Walde SJ. 2012. Emergence of blueberry maggot flies (Diptera: Tephritidae) from mulches and soil at various depths. Environ. Entomol. 41:370–76 101. Renkema JM, Walde SJ, Lynch DH, Cutler GC, MacKenzie K. 2012. Ground beetles (Carabidae) are affected by mulch in organic highbush blueberries. Acta Hortic. 933:447–53 102. Retamales JB, Hancock JF. 2012. Blueberries. Wallingford, UK: CABI 103. Rhodes EM, Liburd OE, England GK. 2012. Effects of southern highbush blueberry cultivar and treatment threshold on flower thrips populations. J. Econ. Entomol. 105:480–89 104. Rice KB, Short BD, Leskey TC. 2017. Development of an attract-and-kill strategy for Drosophila suzukii (Diptera: Drosophilidae): evaluation of attracticidal spheres under laboratory and field conditions. J. Econ. Entomol. 110:535–42

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105. Richards R, Alexander S, Station PNR. 2006. A social history of wild huckleberry harvesting in the Pacific Northwest. Gen. Tech. Rep. PNW-GTR-657, US Dep. Agric., For. Serv., Pac. Northwest Res. Stn., Portland, OR 106. Rocca M, Greco N. 2011. Diversity of herbivorous communities in blueberry crops of different regions of Argentina. Environ. Entomol. 40:247–59 107. Rocca M, Greco NM. 2012. Sampling plans for aphids and their parasitoids in blueberry fields in Argentina. Int. J. Pest Manag. 58:320–29 108. Rodriguez-Saona C, Polk D, Holdcraft R, Chinnasamy D, Mafra Neto A. 2010. SPLAT-OrB reveals competitive attraction as a mechanism of mating disruption in oriental beetle (Coleoptera: Scarabaeidae). Environ. Entomol. 39:1980–89 109. Rodriguez-Saona C, Vincent C, Polk D, Drummond FA. 2015. A review of the blueberry maggot fly (Diptera: Tephritidae). J. Integr. Pest Manag. 6:11 110. Rodriguez-Saona CR, Wise JC, Polk D, Leskey TC, Vandervoort C. 2013. Lethality of reduced-risk insecticides against plum curculio (Coleoptera: Curculionidae) in blueberries, with emphasis on their curative activity. Pest Manag. Sci. 69:1334–45 111. Roth H, Richardson HH. 1970. Ethylene dibromide, methyl bromide, and ethylene chlorobromide as fumigants for control of apple and blueberry maggots in fruit. J. Econ. Entomol. 63:496–99 112. Roubos CR, Liburd OE. 2010. Evaluation of emergence traps for monitoring blueberry gall midge (Diptera: Cecidomyiidae) adults and within field distribution of midge infestation. J. Econ. Entomol. 103:1258–67 113. Sciarappa WJ, Polavarapu S, Holdcraft RJ, Barry JD. 2005. Disruption of sexual communication of oriental beetles (Coleoptera: Scarabaeidae) in highbush blueberries with retrievable pheromone sources. Environ. Entomol. 34:54–58 114. Sharp JL, Polavarapu S. 1999. Gamma radiation doses for preventing pupariation and adult emergence of Rhagoletis mendax (Diptera: Tephritidae). Can. Entomol. 131:549–55 115. Sheppard DH, Myers JH, Fitzpatrick S, Gerber H. 1990. Efficacy of deltamethrin and Bacillus thuringiensis Berliner ssp. kurstaki on larvae of winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae) attacking blueberry in the lower mainland of British Columbia. J. Entomol. Soc. B. C. 87:25–29 116. Smith DC, Prokopy RJ. 1981. Seasonal and diurnal activity of Rhagoletis mendax flies in nature. Ann. Entomol. Soc. Am. 74:462–66 117. Smith JJ, Gavrilovic V, Smitley DR. 2001. Native Vaccinium spp. and Gaylussacia spp. infested by Rhagoletis mendax (Diptera: Tephritidae) in the Great Lakes region: a potential source of inoculum for infestation of cultivated blueberries. J. Econ. Entomol. 94:1378–85 118. Spiers JD, Matta FB, Marshall DA, Sampson BJ. 2005. Effects of kaolin clay application on flower bud development, fruit quality and yield, and flower thrips [Frankliniella spp. (Thysanoptera: Thripidae)] populations of blueberry plants. Small Fruits Rev. 4:73–84 119. Stelinski LL, Liburd OE. 2001. Evaluation of various deployment strategies of imidacloprid-treated spheres in highbush blueberries for control of Rhagoletis mendax (Diptera: Tephritidae). J. Econ. Entomol. 94:905–10 Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. 120. Stelinski LL, Pelz-Stelinski KS, Liburd OE, Gut LJ. 2006. Control strategies for Rhagoletis mendax disrupt host-finding and ovipositional capability of its parasitic wasp, Diachasma alloeum. Biol. Control 36:91–99 121. Strik BC, Yarborough D. 2005. Blueberry production trends in North America, 1992 to 2003, and predictions for growth. HortTechnology 15:391–98 122. Stubbs CS, Drummond FA, Allard SL. 1997. Bee conservation and increasing Osmia spp. in Maine lowbush blueberry fields. Northeast. Nat. 4:133–44 123. Swoboda-Bhattarai KA, Burrack HJ. 2014. Influence of edible fruit coatings on Drosophila suzukii (Mat- sumura) (Diptera: Drosophilidae) oviposition and development. Int. J. Pest Manag. 60:279–86 124. Szendrei Z, Isaacs R. 2006. Ground covers influence the abundance and behavior of Japanese beetles. Environ. Entomol. 35:789–96 125. Szendrei Z, Mallampalli N, Isaacs R. 2005. Effect of tillage on abundance of Japanese beetle, Popillia japonica Newman (Col., Scarabaeidae), larvae and adults in highbush blueberry fields. J. Appl. Entomol. 129:258–64

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126. Teixeira LAF, Polavarapu S. 2001. Postdiapause development and prediction of emergence of female blueberry maggot (Diptera: Tephritidae). Environ. Entomol. 30:925–31 127. Tertuliano M, Srinivasan R, Scherm H. 2012. Settling behavior of the glassy-winged sharpshooter, Homalodisca vitripennis, vector of Xylella fastidiosa, on southern highbush blueberry cultivars. Entomol. Exp. Appl. 143:67–73 128. Tochen S, Dalton DT, Wiman N, Hamm C, Shearer PW, Walton VM. 2014. Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ. Entomol. 43:501–10 129. Tomlinson WE. 1951. Control of insect larvae infesting immature blueberry fruit. J. Econ. Entomol. 44:247–50 130. Tuell JK, Isaacs R. 2010. Community and species-specific responses of wild bees to insect pest control programs applied to a pollinator-dependent crop. J. Econ. Entomol. 103:668–75 131. US Congress. 1996. H.R. 1627: Food Quality Protection Act of 1996. 104th Congr., Aug. 3 132. US Dep. Agric. 1997. United States standards for grades of blueberries. US Dep. Agric., Washington, DC 133. Van Timmeren S, Isaacs R. 2009. Susceptibility of highbush blueberry cultivars to cranberry fruitworm and Japanese beetle. Int. J. Fruit Sci. 9:23–34 134. Van Timmeren S, Isaacs R. 2013. Control of spotted wing drosophila, Drosophila suzukii, by specific insecticides and by conventional and organic crop protection programs. Crop Prot. 54:126–33 135. Vander Kloet SP. 1988. The Genus Vaccinium in North America. Ottawa: Agric. Can. 136. Vera M, Aguilera A, Rebolledo R. 2010. Comparison of relative abundance and diversity of coccinellids (Coleoptera: Coccinellidae) in blueberries (Vaccinium corymbosum L.), under two production systems in the La Araucanıa´ region, Chile. Cienc. Investig. Agrar. 37:123–29 137. Vincent C, Lemoyne P, Gaul S, Mackenzie K. 2014. Extreme cold temperature to kill blueberry maggot (Diptera: Tephritidae) in reusable containers. J. Econ. Entomol. 107:906–9 138. Wallingford AK, Cha DH, Loeb GM. 2017. Evaluating a push-pull strategy for management of Drosophila suzukii Matsumura in red raspberry. Pest Manag. Sci. 74:120–25 139. Walton NJ, Isaacs R. 2011. Influence of native flowering plant strips on natural enemies and herbivores in adjacent blueberry fields. Environ. Entomol. 40:697–705 140. Whalon ME, Elsner EA. 1982. Impact of insecticides on Illinoia pepperi and its predators. J. Econ. Entomol. 75:356–58 141. Whitehouse TS, Sial AA, Schmidt JM. 2018. Natural enemy abundance in southeastern blueberry agro- ecosystems: distance to edge and impact of management practices. Environ. Entomol. 47:32–38 142. Whitney SP, Meyer JR. 1988. Movement between wild and cultivated blueberry by two species of sharpnosed leafhoppers (Homoptera: Cicadellidae) in North Carolina. J. Entomol. Sci. 23:88–95 143. Wiman NG, Parker JE, Rodriguez-Saona C, Walton VM. 2015. Characterizing damage of brown marmorated stink bug (Hemiptera: Pentatomidae) in blueberries. J. Econ. Entomol. 108:1156–63 144. Wise JC, Jenkins PE, Poppen RV, Isaacs R. 2010. Activity of broad-spectrum and reduced-risk insecticides on various life stages of cranberry fruitworm (Lepidoptera: Pyralidae) in highbush blueberry. Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. J. Econ. Entomol. 103:1720–28 145. Wood GW. 1970. Survival of blueberry casebeetle adults in burned blueberry fields. J. Econ. Entomol. 63:1364 146. Wood GW. 1979. Recuperation of native bee populations in blueberry fields exposed to drift of feni- trothion from forest spray operations in New Brunswick. J. Econ. Entomol. 72:36–39 147. Woolwine AE, Culin JD, Gorsuch CS. 1996. Cultivar preference of Oberea myops in rabbiteye blueberries, Vaccinium ashei. J. Agric. Entomol. 13:121–27 148. Wright S, Hu XP, Prokopy RJ. 1997. Tests of imidacloprid-treated spheres for controlling apple maggot flies. Fruit Notes 62:1–4 149. Yarborough D, Drummond F, Annis S, D’Appollonio J. 2017. Maine wild blueberry systems analysis. Acta Hortic. 1180:151–60 150. Zahn DK, Haviland DR, Stanghellini ME, Morse JG. 2013. Evaluation of Beauveria bassiana for management of citrus thrips (Thysanoptera: Thripidae) in California blueberries. J. Econ. Entomol. 106:1986–95

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Annual Review of Entomology

Volume 64, 2019 Contents

An Unlikely Beginning: A Fortunate Life Elizabeth A. Bernays ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Locust and Grasshopper Management Long Zhang, Michel Lecoq, Alexandre Latchininsky, and David Hunter ppppppppppppppppp15 The Ecology of Collective Behavior in Ants Deborah M. Gordon ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp35 Invasion Success and Management Strategies for Social Vespula Wasps Philip J. Lester and Jacqueline R. Beggs ppppppppppppppppppppppppppppppppppppppppppppppppppppp51 Invasive Cereal Aphids of North America: Ecology and Pest Management Michael J. Brewer, Frank B. Peairs, and Norman C. Elliott ppppppppppppppppppppppppppppppp73 Blueberry IPM: Past Successes and Future Challenges Cesar Rodriguez-Saona, Charles Vincent, and Rufus Isaacs pppppppppppppppppppppppppppppppp95 Development of Baits for Population Management of Subterranean Termites Nan-Yao Su pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp115 Biology and Control of the Khapra Beetle, Trogoderma granarium,a Major Quarantine Threat to Global Food Security Christos G. Athanassiou, Thomas W. Phillips, and Waqas Wakil ppppppppppppppppppppppp131 Vectors of Babesiosis Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. Jeremy S. Gray, Agust´ın Estrada-Pe˜na, and Annetta Zintl pppppppppppppppppppppppppppppp149 Movement and Demography of At-Risk Butterﬂies: Building Blocks for Conservation Cheryl B. Schultz, Nick M. Haddad, Erica H. Henry, and Elizabeth E. Crone ppppppppp167 Epigenetics in Insects: Genome Regulation and the Generation of Phenotypic Diversity Karl M. Glastad, Brendan G. Hunt, and Michael A.D. Goodisman ppppppppppppppppppppp185 Bee Viruses: Ecology, Pathogenicity, and Impacts Christina M. Grozinger and Michelle L. Flenniken pppppppppppppppppppppppppppppppppppppp205

viii EN64_FrontMatter ARI 4 December 2018 14:41

Molecular Evolution of the Major Arthropod Chemoreceptor Gene Families Hugh M. Robertson pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp227 Life and Death at the Voltage-Sensitive Sodium Channel: Evolution in Response to Insecticide Use Jeffrey G. Scott pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp243 Nonreproductive Effects of Insect Parasitoids on Their Hosts Paul K. Abram, Jacques Brodeur, Alberto Urbaneja, and Alejandro Tena pppppppppppppp259 Movement Ecology of Pest Helicoverpa: Implications for Ongoing Spread Christopher M. Jones, Hazel Parry, Wee Tek Tay, Don R. Reynolds, and Jason W. Chapman pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp277 Molecular Mechanisms of Wing Polymorphism in Insects Chuan-Xi Zhang, Jennifer A. Brisson, and Hai-Jun Xu ppppppppppppppppppppppppppppppppp297 Fat Body Biology in the Last Decade Sheng Li, Xiaoqiang Yu, and Qili Feng ppppppppppppppppppppppppppppppppppppppppppppppppppp315 Systematics, Phylogeny, and Evolution of Braconid Wasps: 30 Years of Progress Xue-xin Chen and Cornelis van Achterberg ppppppppppppppppppppppppppppppppppppppppppppppp335 Water Beetles as Models in Ecology and Evolution David T. Bilton, Ignacio Ribera, and Andrew Edward Z. Short ppppppppppppppppppppppppp359 Phylogeography of Ticks (Acari: Ixodida) Lorenza Beati and Hans Klompen pppppppppppppppppppppppppppppppppppppppppppppppppppppppppp379

Indexes

Cumulative Index of Contributing Authors, Volumes 55–64 ppppppppppppppppppppppppppp399 Cumulative Index of Article Titles, Volumes 55–64 ppppppppppppppppppppppppppppppppppppp404 Annu. Rev. Entomol. 2019.64:95-114. Downloaded from www.annualreviews.org Access provided by CASA Institution Identity on 10/08/20. For personal use only. Errata

An online log of corrections to Annual Review of Entomology articles may be found at http://www.annualreviews.org/errata/ento

Contents ix