entomological opportunities and challenges for … opportunities and challenges for sustainable ......

EN63CH11-Daane ARI 20 November 2017 12:1

Annual Review of Entomology

Entomological Opportunitiesand Challenges for SustainableViticulture in a Global MarketKent M. Daane,1,∗ Charles Vincent,2 Rufus Isaacs,3

and Claudio Ioriatti41Department of Environmental Science, Policy, and Management, University of California,Berkeley, California 94720-3114; email: [email protected] Research and Development Centre, Agriculture Agri-Food Canada,Saint-Jean-sur-Richelieu, Quebec J3B 3E6, Canada; email: [email protected] of Entomology, Michigan State University, East Lansing, Michigan 48824;email: [email protected] Transfer Center, Fondazione Edmund Mach, San Michele all’Adige,Trento 38010, Italy; email: [email protected]

Annu. Rev. Entomol. 2018. 63:193–214

The Annual Review of Entomology is online atento.annualreviews.org

https://doi.org/10.1146/annurev-ento-010715-023547

Copyright c© 2018 by Annual Reviews.All rights reserved

This paper was authored by an employee of theCanadian Government as part of his official dutiesand is therefore subject to Crown Copyright.Reproduced with the permission of the Controllerof Her Majesty’s Stationery Office/Queen’sPrinter for Agriculture and Agri-Food Canada andthe Saint-Jean-sur-Richelieu Research andDevelopment Centre.

∗Corresponding author

Keywords

grape pest management, global trade, invasive species, vineyard

Abstract

Viticulture has experienced dramatic global growth in acreage and value. Asthe international exchange of goods has increased, so too has the marketdemand for sustainably produced products. Both elements redefine the en-tomological challenges posed to viticulture and have stimulated significantadvances in arthropod pest control programs. Vineyard managers on all con-tinents are increasingly combating invasive species, resulting in the adoptionof novel insecticides, semiochemicals, and molecular tools to support sustain-able viticulture. At the local level, vineyard management practices considerfactors such as the surrounding natural ecosystem, risk to fish populations,and air quality. Coordinated multinational responses to pest invasion havebeen highly effective and have, for example, resulted in eradication of themoth Lobesia botrana from California vineyards, a pest found in 2009 anderadicated by 2016. At the global level, the shared pests and solutions fortheir suppression will play an increasing role in delivering internationallysensitive pest management programs that respond to invasive pests, climatechange, novel vector and pathogen relationships, and pesticide restrictions.

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ANNUAL REVIEWS Further

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http://www.annualreviews.org/doi/full/10.1146/annurev-ento-010715-023547


INTRODUCTION

Grape production is aimed at various markets—namely, table grapes for fresh consumption andprocessed grapes that are dried into raisins or pressed for grape juice or wine. Viticulture is thecultivation, protection, and harvesting of grapes (outdoor occupations), whereas enology is thefermentation of grapes into wine (indoor occupations). The grape industry experienced one ofthe highest levels of economic growth among agricultural commodities over the past 30 years,and grape and wine production is now a global multibillion dollar enterprise (20). This growthis related to factors such as increased international trade, improved global incomes, changingpolicies, and remarkable technological innovations in production, storage, and transportation.Increased consumer demand for fruits and vegetables is also associated with greater awareness ofthe health benefits of foods providing antioxidants, such as grapes (150).

Grapes have a long history of cultivation and breeding for a wide range of soils and climates.Vineyards are found in all continents and in climates ranging from tropical to temperate to desertregions (Figure 1). In some parts of the world, grape acreage has decreased, whereas in other re-gions, acreage and production have expanded to a massive extent (Supplemental Element 1), re-sulting in greater international trade, driven in part by increasing consumption of fresh grapes. Thisis reflected in California, where annual per capita table grape consumption grew from 1.8 to 3.5 kgbetween 1980 and 2001. The United States is still a net importer of table grapes, despite Californiaproducing 71,000 tons of table grapes out of the 3,862,000 tons harvested globally in 2015 (30).

a Grape area (in 1,000 hectares)

5–40 40–100 100–200 200–300

China

Italy

USA

France

Spain

Turkey

Chile India

Argentina

Iran

Australia

Egypt

SouthAfrica

Brazil

Germany

b Production (in 1,000 tons)

7,500 5,000 1,00010,000 2,500

c Type of grape

Wine (excluding juice) Dried (raisin) Fresh (table)

300–500 500–750 >750

Canada

NewZealand

Mexico

Figure 1Major grape production of the world showing (a) the land area planted to vineyards, (b) the grape fruit production from each of the 18most productive countries, and (c) the percentage of the grape commodity (wine, dried fruit, and fresh fruit) in each of the 15 mostproductive countries. Adapted from Reference 109, with permission.

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Supplemental Material

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http://www.annualreviews.org/doi/suppl/10.1146/annurev-ento-010715-023547


The greater production and movement of fresh grapes around the globe create opportunitiesfor arthropod pest and pathogen invasions to new regions, despite phytosanitary inspections.Along with the rapid globalization of grape commodities, there has been extensive movement ofplant material to provide new rootstocks and cultivars to keep pace with industry demands. Pestscan also be spread through the exchange of machinery; this practice is generally limited to localmovement, but it can facilitate long-distance movement such as when harvesting machines aremoved between hemispheres for two harvests per year.

There is also increasing public demand for sustainable farming practices, compelling man-agers to reach targets for carbon neutrality, water use reduction, and integrated pest management(83) and fostering regional programs to develop sustainability goals (146), including certificationand labeling to inform buyers of viticultural practices used. Currently, the concept of sustainableviticulture, including guidelines for integrated production of grapes, requires that the industry op-timize available resources to improve environmentally responsible viticulture (96). For example,mitigation of the effects of climate change rely on an array of farming practices (e.g., tillage, varietyand rootstock, and irrigation) and applying guidelines for integrated viticulture production (e.g.,International Organization for Biological Control guidelines). For grape production to be sus-tainable, it must address the challenges posed by arthropod pests, so monitoring and managementprograms should include flexibility and resiliency to respond to existing and future challenges.

There have been numerous disruptive invasions by arthropod pests into grape production thathave threatened sustainability. Their arrival often leads to higher management costs, lower yields,and greater environmental impact as managers and researchers respond to the urgent need toaddress new pest challenges. Often, a short-term insecticide-based response is required while al-ternative control tools such as mating disruption and biological control are developed. Many of themost challenging invasive pests of global grape production have, however, been well studied in theirhome range, which can provide exceptionally valuable information for mounting rapid responsesfor control. An early example was the transfer of knowledge about rootstock resistance to phyl-loxera (Daktulosphaira vitifoliae) that helped save the French and then North American winegrapeindustries (25). With greater and more rapid communication among researchers, opportunitiesfor knowledge transfer following pest invasion are far superior today than even just a decade ago.If political and financial resources are available, rapid response to pest invasion greatly increasesopportunities for successful eradication. An excellent example is the response to the Europeangrapevine moth (Lobesia botrana) in California after its detection in 2009 (138), which was helpedimmensely by the involvement of European experts with experience managing this pest (39, 91).

This review focuses on entomological challenges, including invasive species, to sustainableviticulture in a global market. The changing climate is also expected to interact with the threat ofpest invasion, providing expanded ranges for viticulture as well as influencing the range of somekey pests. Situations where climate change effects are already documented are described, withprojections for the long-term importance of these changes for grape pest management.

INVASIVE SPECIES AND GRAPE PRODUCTION

The growing international trade in vines, grapes, and equipment causes increased opportunity foraccidental movement of invasive pests and pathogens. Here, we discuss how grapes, in particular,are at increased risk for the movement of invasive insect species because of this global exchange.

Movement of Plant Material

Grapevines shipped among adjacent regions and internationally must comply with phytosanitaryand quarantine regulations. For Vitis plant material, these are highly variable among different

www.annualreviews.org • Entomological Opportunities and Challenges 195

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jurisdictions. Some of the reasons are historical, but, in general, newer grape-growing regionshave fewer arthropod and pathogen problems than the older regions. These new regions (e.g.,New Zealand, Australia, Canada) are more likely to protect their industry from inadvertent intro-ductions of exotic pests from older regions (e.g., Mediterranean countries). Some of the strictestregulations for Vitis are found in Australia, Chile, New Zealand, South Africa, and the UnitedStates, where importation of new plant material may take years (62). The Food and AgricultureOrganization of the United Nations works to harmonize standards for the international move-ment of plant material, but international trade in unprocessed fruit and vines still occurs and isthe main source of pest dissemination. Pest introduction rates are climbing, with a doubling inrecent decades, suggesting that globalization is enhancing rates of pest movement (139). Despiteinternational cooperation, decisions on specific pest status and developing effective regulations toaddress each pest species can be slow, and once regulations are in place, the border inspectionsmay not be adequate (93). Moreover, the sheer volume of plant material moved among regionsmakes detection of all potential pests highly unlikely.

Shared Pest Problems

Global commerce will increase pest introductions into new regions, where pests may find abundanthost plants and disrupt existing pest control programs. There are numerous examples in recentyears, such as the range expansion and pest status of the spotted-wing drosophila (Drosophilasuzukii) (6). This fly has a specialized ovipositor that enables it to infest grape varieties that havesofter berries, resulting in direct damage and the transfer of pathogens that can affect wine quality(36, 75). The brown marmorated stink bug (Halyomorpha halys) is another example; adults aggre-gate in grape clusters during harvest, posing significant risks to the quality of harvested grapesbecause of their release of pungent alkaloids (105). Smith et al. (128) found a direct correlationbetween H. halys density and grape yield loss. This insect has become increasingly importantin the eastern United States (128) and Europe (147), and, because H. halys populations are stillexpanding (69), their full economic impact in vineyards remains to be seen (158). Similarly, theAsian lady beetle (Harmonia axyridis)—a predator deliberately introduced into North Americaand Europe for biocontrol purposes—can be a pest when pressed with grapes because it releasesalkyl methoxypyrazines that taint wine (141). A final example is the spotted lanternfly (Lycormadelicatula), which was first detected in the New World in 2014 in Pennsylvania (10). Eradica-tion programs are being implemented to contain its spread, in part because of the risk to thegrape industry, but new infestations continue to be detected. Previously limited to their nativeranges, these insects and others have demonstrated a remarkable ability to cause economic damage(Supplemental Element 2).

Insect Vectors

In most wine grape regions, the transmission of plant pathogens, rather than insect feeding damage,is the primary concern (33, 145). Key among pathogens are Grapevine leafroll-associated viruses(GLRaVs) (3), which can be damaging to vines, crop, and wine quality (2, 100). It was demonstratedthat several mealybug and scale species are the primary GLRaV vectors, including common speciessuch as Pseudococcus maritimus, Ps. viburni, Planococcus ficus, Pl. citri, and Parthenolecanium corni thathave spread to many global grape regions (3). Although all stages may transmit GLRaV-3, thefirst instars appear to be more efficient vectors (134) and are also the dispersal stage, with crawlersoften being carried by the wind (9) and crawlers and other stages also being moved on equipmentand infested nursery stock (68). Control is further hampered as mealybugs can survive on andviruses can survive in vine roots for years after the vine aboveground has been pulled (12, 145).

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The difficulty of controlling GLRaV vectors often disrupts sustainability programs as farmersadopt a zero tolerance for vector species and a greater reliance on insecticides to reduce vectorsto slow pathogen spread (85, 142).

More recent examples during the past decade include a new or long-hidden red leaf pathogenknown as Grapevine red blotch associated virus (GRBaV) (1, 87). Evidence points to membracidsfeeding primarily on vegetation in or near vineyards as the most likely vectors (7). Another re-cently identified virus is Grapevine Pinot gris virus (GPGV), first identified in Italy in 2012 and thenreported in other European countries, China, and Korea (59). The grape erineum mite, Colomerusvitis, was demonstrated to transmit GPGV to healthy grapevines (94), but GPGV spread also in-volves movement of nursery material. In these examples, even low incidence of vector or pathogenoften leads to insecticide applications—even before the life cycle of the vectors, their ecology, orthe vector–pathogen–plant interactions are fully understood—and highlights the increased aware-ness of damage from invasive species that are also insect vectors.

SUSTAINABLE PEST MANAGEMENT TOOLS

Concurrent with the increase in invasive vineyard pests, there has been greater farmer interest andpublic demand for sustainable farming practices. Researchers and farmers have met this challengeby improving pest management practices, developing novel control tools, and implementing newsolutions, such as areawide pest management.

Transition to Sustainable Pest Management

Grape pest management has advanced through various phases over the past century (78), andvineyard systems have often led the development of new technologies for insect control, such asrootstocks for effective pest resistance against phylloxera and pheromone-based mating disruption.Because of their high value, grapes are often included in the initial registrations for new reduced-risk insecticides, providing opportunities to lower the environmental load and improve the safetyof integrated pest management programs to workers.

Biological Controls and Biodiversity

For many perennial crops, natural enemies are a primary tool of sustainable pest management.The best examples of classical biological control in vineyards are with hemipterans. The NorthAmerican flatid Metcalfa pruinosa was first detected in Europe in 1970 in Treviso, Italy (157). Itquickly spread through Italy and to some neighboring countries (155), infesting forest stands andcrops, including grapes (73). Complete control of this invasive pest was achieved by releasing theNorth American dryinid predator Neodryinus typhlocybae (61, 101).

Mealybugs have often been targeted for biocontrol; for example, the encyrtid Anagyrus pseudo-cocci has been used around the world to suppress Pl. citri and Pl. ficus (46, 55, 63). In New Zealand,Ps. viburni was brought under exceptional control by release of the encyrtid Pseudaphycus mac-ulipennis (32). Not surprisingly, ants that rely on mealybugs as a source of honeydew can disruptmealybug biocontrol (48, 102), leading to investigations of more sustainable controls for commonant species, such as the Argentine ant (Linepithema humile) (38, 49).

Supporting biodiversity is an increasingly common approach in sustainable systems (79, 88,127); this includes enhancing floral diversity inside vineyards (22, 153). One approach is to plantannual cover crops that bloom quickly that year (11, 14, 42) and then can be cut or incorporatedinto the soil to provide soil nutrients (86). Vineyards planted with flowering buckwheat (Fagopyrumesculentum), for example, had higher leafhopper egg parasitism in New York (United States) (54)


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and higher leafroller larval parasitism in New Zealand (13). This tactic is more common in regionswith regular rainfall that support growth of grasses and broadleaf cover crops, such as clover, whichprovide resources for beneficial insects and are easily managed with tilling, mowing, or herbicides.There is also increasing interest in adding native perennial flowering plants into landscapes (56,81), in part because the aesthetic benefits can enhance a winery’s marketing.

Biodiversity in vineyards is influenced by the surrounding habitat, and natural enemy abundanceis often positively correlated with nearby woody vegetation (71, 107, 114, 131). For example, somemymarid egg parasitoids (Anagrus spp.) of leafhopper pests overwinter in eggs of alternate hostsfound in natural habitats outside the vineyard (90, 151, 154). In Germany, planting dog roses (Rosacanina) near vineyards provided habitat for Anagrus atomus, a natural enemy of the leafhopperEmpoasca vitis (16, 17), and in California, vineyards close to patches of blackberry (Rubus spp.) havehigher Anagrus parasitism rates of the leafhopper Erythroneura elegantula (53).

Still, increasing biodiversity does not always produce the desired results, and competition withvines for soil resources is also possible (86). In northern Italy, increased biodiversity did notincrease egg parasitoids of the leafhopper Scaphoideus titanus (119), whereas in Switzerland, theaddition of hedgerows provided important overwintering habitats for the mymarid parasitoids A.atomus and Stethynium triclavatum (118). Some vineyard ground covers can indirectly influenceleafhopper densities by lowering vine vigor and thereby reducing the vine’s host suitability (42,152). The inconsistent results after increasing biodiversity suggest that arthropod biology andecology, or vineyard and landscape structure, present complex ecosystems that can require morespecific manipulations than simply increasing biodiversity to provide desired ecosystem services.

Novel Pesticides and International Trade

Pesticides are common components of grape production and can be important tools in modernsustainable systems (19). The development of insecticide resistance (34, 57) and secondary pestproblems (52, 144) have fostered development and use of more selective programs (122, 136). Evenapplications of fungicides for disease control can harm beneficial insects (130). In the past decade,fewer new insecticides have been registered for use in vineyards, but a notable exception is thebutenolide flupyradifurone, which exhibits activity on mealybugs (106), providing an additionaloption to control homopteran pests and manage insecticide resistance. Moreover, this insecticideprovides a safer profile for bees than most neonicotinoids used in vineyards, allowing control ofsome key pests with minimal impact on beneficial insects (26).

In the past few decades, more selective and less disruptive insecticides, including some neo-nicotinoids, insect growth regulators, and tetramic acids, have replaced the broad-spectrum in-secticides in many regions of grape production. For lepidopteran pests, ecdysone agonists suchas methoxyfenozide provide selective disruption of moth development, with activity on multiplelife stages of key New and Old World vineyard pests and with low impact on natural enemies(27, 77, 124). The tetramic acid spirotetramat has shown excellent activity against challengingpests, including mealybugs, phylloxera, and scales (21), resulting in reduced spread of grapevineleafroll-associated virus (142), with limited effects on some natural enemies (99).

Adoption of sustainable practices may also have benefits in terms of access to international mar-kets. As grapes and grape products are moved across international borders, they are subject to pesti-cide residue tests. These must be below the maximum residue limit (MRL) for each pesticide or theshipment cannot enter. MRLs are set separately by each country for each pesticide, and the levelscan vary widely among countries despite recent efforts at international harmonization (66). Pesti-cide residues have been characterized for grape products (reviewed in Reference 23), showing muchlower levels in processed than fresh products. Regions with low MRL values (for example, Europe)

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influence which pesticides are used and their timing of application relative to harvest, especially forfresh grapes. In countries with large grape export businesses, research has revealed how residues de-cline after application (121), and this information can guide decision-making to avoid MRL viola-tions (97). Differences in pesticide registration standards, delays in compliance assessment, and di-vergence in pesticide MRLs constitute technical barriers impeding international grape trade (148).

Semiochemicals

Pheromone mating disruption fits well in an areawide pest management (AWPM) approach andwas successfully used to improve control of two important European moth pests (L. botrana andEupoecilia ambiguella) (73). Following the first detection of L. botrana in North America, areawidemating disruption became an important component of the management and eradication strategy,in conjunction with insecticides applied to cultivated areas and grape removal from uncultivatedareas (91). This provides an example of the global development of a pest management program,as the use of sex pheromones for L. botrana was conceptually conceived in Europe (72) manydecades before the sex pheromones’ chemical structures were discovered in the United States(120). The field development of this tool occurred in Europe, where L. botrana mating disruptionis now applied on ∼140,000 hectares, or about 3–4% of the grape-growing area, providing a highlyselective and environmentally acceptable control tool (74). The decades of experience with matingdisruption in European vineyards were invaluable when L. botrana was first detected in Chile in2008, California in 2009, and Argentina in 2010 (39, 74).

Sustainable Programs

The conventional approach to pest management has been to treat individual vineyards beforean economically damaging pest infestation develops (140). Insects do not recognize individualvineyard boundaries, so managing them over a broader spatial extent may be more effective. Thisconcept is the essence of AWPM, in which management tactics are applied over many vineyards,adjacent farms, or whole regions, often treated simultaneously. Whereas the aim is typically tomaintain the pest below economic levels, in some cases, this approach is central to achieve completeeradication of an invasive pest.

AWPM is fully compatible with, and complementary to, the sustainable controls mentionedpreviously: biological controls and enhanced biodiversity, target-specific insecticides, semiochem-icals, and other sustainable management tactics. AWPM has potential advantages over the con-ventional approach. Suppression across a broad area may result in reduced reinfestation by immi-gration from unmanaged areas, and the pest management tactics employed may be more effective,particularly ecologically based tactics, when applied at this scale (31). The first example of anAWPM in vineyards was against phylloxera in Europe during the 1870s, using resistant grapevines(115). Another early example is a provincial law passed on April 30, 1870, in the Trentino–SouthTyrol region that ordered the first mandatory control measure for collecting L. botrana larvae. Arecent example of mandatory application of AWPM began in 2000 and concerns the required useof insecticide sprays against the leafhopper Scaphoideus titanus, which has invaded several Europeancountries and poses a threat as a vector of the phytoplasma of flavescence doree (35).

MARKET DEMAND FOR SUSTAINABLE VITICULTURE

At the global level, the shared pests and solutions for their suppression will play an increasing rolein delivering internationally sensitive pest management programs that respond to invasive pests,climate change, novel vector and pathogen relationships, and pesticide restrictions.


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EnvironmentalNatural resource use

Environmental managementPollution prevention (air, water,

land, waste, pesticides)

EconomicResearch and development

ProfitCost savings

Economic growth

Social Standard of living

EducationCommunity

Equal opportunity

Economic–socialBusiness ethics

Fair tradeWorkers’ rights

Environmental–economicEnergy efficiency

Subsidies/incentives foruse of natural resources

Social–environmentalEnvironmental justice

Natural resource stewardshiplocally and globally

Arthropoddiversity

Biological controlwith arthropods

Shared pest challenges

National and internationalregulations

(quarantine, pesticides)

International trade(table grapes, vines,

nursery material)

SUSTAINABILITY

Figure 2The interrelationships of social, environmental, and economic components of sustainability in the grape andwine industries. Blue text signifies entomological issues addressed within this review. Adapted fromReference 83 with permission.

Interrelationships in Sustainable Viticulture

Sustainable viticulture is defined as a “global strategy on the scale of the grape production andprocessing systems, incorporating at the same time the economic sustainability of structures andterritories, producing quality products, considering requirements of precision in sustainable viti-culture, risks to the environment, product safety and consumer health and valuing of heritage,historical, cultural, ecological and landscape aspects” (76). The concept encompasses three compo-nents: economic (maximization of welfare and improvement of efficiency), social (interregional andintergenerational equities), and environmental (conservation of resources and functioning withincarrying capacities of agroecosystems) (Figure 2). Interactions such as environmental–economicfactors address concerns such as energy efficiency and subsidies/incentives for use of natural re-sources (Figure 2). Viticultural entomology belongs to the environmental–economic interactionbecause deliberate measures to limit insecticides will increase entomological biodiversity, mitigateenvironmental damage, and lower input costs.

Certification Programs

Sustainability programs generally include protocols (defined sets of procedures), managementtools (used for assessment and improvement), and indicators (that express a concise and compara-tive measure—for example, carbon or water footprint). A program may also require participating

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wineries to validate protocol compliance by program staff or a third party that assesses the threesustainability components (108) (Figure 2). The outcome of the validation process is certification.Some programs adopt a certification label (affixed to the wine bottle) informing consumers aboutthe sustainability of the product (40). The motivations for adopting a sustainability program rangefrom environmental concerns to the added economic value of the product or land (50). Althoughtypical wine consumers are well educated and affluent, they may be less knowledgeable aboutsustainable production (113), and the perception of the producer as a responsible environmentalsteward can influence the consumer’s purchasing decision (60, 126).

Global Standards

The markets for organic or biodynamic wines have increased globally in response to increasedenvironmental awareness. Sustainability programs were pioneered in New World wine countries,such as Australia, Chile, New Zealand, South Africa, and the United States (125), with their effortsoften focused on environmentally friendly labeling and green production practices (126). It wasonly in 2012 that Europe defined “organic wine” and, traditionally, European wine countries reliedon other differentiation mechanisms to position their wines—for example, the concept of terroir inFrance and the Denominazione di Origine Controllata in Italy. However, some European countriesare making progress in defining or implementing sustainability programs (40). European wineriesare currently focusing on consumer perception and willingness to pay a premium for organic wine.China now has the second-largest vineyard area in the world (Figure 1), and 80% of its wine is con-sumed domestically (89). The wine and grape industries of China are facing several challenges, in-cluding development of a classification system for wine and sustainability programs to support thisindustry; however, literature related to sustainable viticulture in China is rare and difficult to obtain.

Santiago-Brown et al. (125) reviewed notable sustainability programs (Table 1) and concludedthat (a) there are no global standards defining sustainable viticulture; (b) the environmental compo-nent is important at the beginning of most programs but, over time, its importance declines in favorof economic and social components; and (c) entomological considerations vary across programs.Among these programs, the Lodi Rules for Sustainable Winegrowing was developed by Califor-nia’s Lodi Winegrape Commission and has a strong pest management component (108). Initially,growers faced three challenges: define sustainable viticulture, implement it, and measure its impact.The group identified 105 issues distributed across seven categories: viticulture, soil management,pest management, water management, habitat, human resources, and wine quality. The programresulted in participating growers increasing their adoption of practices such as monitoring forpests (such as leafhoppers, mealybugs, and moths) and beneficial insects (such as green lacewingsand mealybug parasitoids), use of cover crops for natural enemy refuges, alternate row spraying,use of pheromones for specific pests (such as Pl. ficus and Platynota stultana), and leaf pulling.

Another program that had a strong entomological component is the Greening Waipara Projectof New Zealand (43). It introduced seven environmental innovations for vineyards and winer-ies to adopt—notably, biological control practices for management of tortricid leafrollers thatcause leaf and fruit damage and increase berry infection by the fungus Botrytis cinerea. Leafrollerswere previously managed by broad-spectrum insecticides, but planting buckwheat added floralresource subsidies that helped support 22 parasitoid species, the most abundant being the bra-conid Dolichogenidea tasmanica (14). Buckwheat was associated with increased larval parasitism,but a leafroller reduction was not consistently demonstrated (14). Several years later, Cullenet al. (43) surveyed Waipara vineyards and found that growers did not continue to practice mostof the environmental innovations, including the addition of buckwheat, indicating the need tocontinually refine sustainable practices to fit into practical vineyard management.


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Table 1 Comparison of selected sustainable viticulture programsa

Program Country Regional scopeYear

startedYear

certified

Vineyardarea

(hectares)Educationalobjectives

Prohibitedchemical list

McLaren ValeSustainableWinegrowing

Australia Regional inMcLaren Valley

2009 2012 2,929b Yes Yes; adopted fromAustralian WineResearch Institute

SustainableWine Chile

Chile National 2009 2011 NA Yes Yes; for herbicides

SustainableWinegrowingNew Zealand

NewZealand

National 2000 2000 33,600 Yes Yes; from NewZealand legislation

IntegratedProduction ofWine

SouthAfrica

National 2010 2010 93,155c Yes Yes

Low InputViticultureandEnology

USA Regional inOregon andWashingtonstate

1999 1999 4,305 Yes Yes; two distinct listsbased on climate ofvineyard location

LodiWinegrowers’Workbook

USA Regional in Lodi/Woodbridge,California

2005 2005 NA Yes PesticideEnvironmentalAssessment Systemrequirements (LodiRules)

VineBalance USA Regional in NewYork

2005 NA 2,658 Yes NA

Vineyard Team/Sustainabilityin Practice

USA Regional inCalifornia

2008 2008 32,375 Yes Yes; high-riskpesticides are notallowed

SustainableWinegrowingProgram

USA Regional inCalifornia

2010 2010 118,736d Yes No

Grape∗A∗Syst USA Regional inMichigan

2009 2009 5,000 Yes No

NA indicates that the data are not available.aAdapted from Reference 125.b39% of total vineyard area in McLaren Valley.c92.6% of total vineyard area in South Africa in 2011.d69% of total wine grape area in California.

The current literature on sustainable viticulture often overlooks points that have entomologicaland strategic relevance. Worldwide, most emerging entomological problems in vineyards arelinked to significant increases in international trade. The risk associated with trading bottles ofwine is nil, whereas risks are keenly associated with trade of living plant material. For example,trading table grapes among major production regions may allow pests endemic to one area tobe transported to areas where they are absent. National and international regulations related toquarantine and pesticide registrations differ from one country to another. The same is true forvines. In Canada, for example, the demand for plant material systematically outpaced the capacity

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of nurseries to produce vines in the last decade. Thus, imports of nursery material exposed Canadato the entry of flavescence doree and bois noir, two serious diseases caused by phytoplasmas andvectored by cicadellids. At the present time, Canada is free of these diseases (110) thanks to thestrict enforcement of import regulations.

OUTCOME OF GLOBALLY SHARED PEST PROBLEMSAND SOLUTIONS

This review has described how increased global commerce may increase pest introductions intonew regions. However, a clearly positive aspect of global exchange is the sharing of knowledge andnovel tools to control invasive pests. The continued development and exchange of pest detectionand management may both help to reduce the accidental dissemination of pests, and improve theirrapid identification and control when invasions do occur.

Impact of Shared Information

Eradication of invasive insects is warranted when the costs of long-term management exceed thoseof eradication (129). Two experiences in California in the past decade demonstrate the power ofcoordinated international efforts to manage invasive pests in viticulture and provide examples ofhow international collaboration can lead to shared benefits.

After the first detection of L. botrana in California in 2009, an eradication program was estab-lished (39, 74). California county and state and federal agencies immediately evaluated the extentof L. botrana populations. A group of local and international experts was formed to manage theemergency and provide urgent recommendations. Within a year, an eradication program was de-veloped (91) and focused on (a) identification of the insect’s geographic range, (b) development andimplementation of detection and eradication programs, including chemical treatment and mat-ing disruption, (c) regulation of grape plant movement to minimize dispersal, (d) incorporatingresearch-based information into policy decisions, and (e) promoting a wide-reaching educationalprogram for growers, the public, and local officials (39). Proposed control efforts consisted ofa robust monitoring program, use of effective insecticides and mating disruption, and restrictedmovement of plant material from infested regions. Organic vineyards and residential areas weretreated with Bacillus thuringiensis, mating disruption, and fruit stripping. This aggressive programcoupled with a high level of public and grower compliance had immediate effects (39, 137), and theeradication of L. botrana in California was declared complete in 2016 (Supplemental Element 3).

The invasive mealybug Pl. ficus probably reached California vineyards with plant materialillegally moved into the state, and then spread within the state from infested nursery material (68).Unlike L. botrana, this invasive mealybug was not a major pest in the Mediterranean region, andthere were no established protocols in Europe for its eradication or suppression in California. Sincethen, management tools were developed to detect population density and predict berry damage(70, 104), effectively use more selective neonicotinoids and tetramic acid insecticides (45, 145),and commercially develop a pheromone mating disruption program (143). These results were astarting point for further development of mating disruption strategies that spread back to Europeand Israel (37, 156), the pest’s presumptive native range. When used in an AWPM program,mating disruption has the added benefit of increasing biocontrol, as Pl. ficus’s pheromone is usedas a kairomone by the encyrtid parasitoid Anagyrus pseudococci (58, 98), which is often limited inits effectiveness by its biology and the mealybug’s location in protected areas of the vine (46, 65).

It is clear from these two examples that international expertise is highly valuable for rapid andeffective responses to pest invasion. There will be increasing need for this type of informationexchange as pest distributions expand and viruses are moved by some of these insects. Cooperation



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between regions, states, and nations should be encouraged to help maintain clean plant materialsand to focus on prevention rather than postdetection responses that are typically much morecostly (92).

Molecular Identification of Novel Pests

Molecular analyses provide a useful and reliable tool for improved insect identification (4). Theseinclude several methods based on polymerase chain reaction (PCR) amplification, including spe-cific primer sets to verify the presence of an amplicon via electrophoresis, restriction enzymes todigest a targeted amplicon generating restriction fragment length polymorphisms (RFLP), ran-dom PCR primers (random amplified polymorphic DNA, or RAPD), amplified fragment lengthpolymorphism (AFLP), multiplex PCR assays (two or more specific primer sets in a single reac-tion), and sequencing to utilize methods such as DNA barcoding (82). For example, moleculartools have been used to distinguish vineyard mealybug species (67, 95), with PCR first used toidentify closely related mealybugs by Beuning et al. (15) in New Zealand and more recently todistinguish Brazilian species (44). RFLP analysis was used for separation of Pl. ficus and Pl. citri(29, 51), and multiplex PCR was used to separate three mealybug species in South Africa (123)and seven species in California (47).

Molecular tools have also been used to determine the origin of invasive species—for example,to support the hypothesis that Ps. viburni is native to South America (41) and to characterizepopulations of L. botrana in Europe and the Middle East (116). Molecular tools will undoubtedlybecome more common and broad in scope in vineyard pest management. Transmission efficiencystudies of GLRaV by mealybugs, for example, were facilitated by the use of quantitative polymerasechain reaction (qPCR) to identify the pathogen in tested insects (134), and identification of thethree-cornered alfalfa tree hopper (Spissistilus festinus) as a vector of GRBaV was aided by the use ofdigital PCR (7). These tools also offer promise to improve sustainable agriculture programs. RFLPwas successfully used to distinguish among larval stages of parasitoid species attacking L. botrana(111), and gene editing tools have been proposed for manipulating natural enemy biology orplant defenses (64). Finally, as regulatory bodies have debated the use and definition of geneticallymodified organisms, researchers have investigated the application of RNA interference to turnoff or silence unwanted or harmful genes in specific plant pathogens or insects (112, 135). Oncedeveloped, these molecular tools can be easily shared globally.

Preparing for Climate Change

Climate change continues to affect viticulture as it has done for thousands of years. Vineyards wereplanted as far north as the coastal zones of the Baltic Sea and southern England during the medievalLittle Climatic Optimum period (roughly 900–1300 AD) when annual average temperatures wereup to 1◦C warmer (83). Numerous wine-growing regions across the globe have warmed recently(84, 149), and phenological changes observed over the last 50 years at numerous locations indicatethat grapevines have responded with earlier bud break, bloom, veraison (onset of ripening), andharvest, resulting in greater risk of frost injury in spring or prolonged berry maturation than inthe past when earlier fall frosts occurred (84). Therefore, the quality and quantity of wines (i.e.,prices and revenues) are extremely sensitive to local weather conditions (5).

Effects of climate change on insect herbivores can be direct through impacts on their physiologyand behavior, or indirect as when the insects respond to climate-induced changes mediated throughother factors, notably the host plant (8). Because climate change can influence the rate of both hostand pest development, it could disrupt their synchrony (24). For example, simulations suggest thatincreasing temperature will increase vine susceptibility to L. botrana in some European regions as a

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result of increased asynchrony between the larva-resistant stages of grapevines and larvae (72). Asan example, voltinism of the grape berry moth (Paralobesia viteana) is sensitive to climate variationamong years (133) and first-generation adults are predicted to emerge from overwintering pupaesooner than in the past, which is predicted to result in oviposition by subsequent generations havinga shift in mean voltinism from 2.8 to 3.6 generations per year by the end of this century. Anotherexample predicts an increase in population size and distribution of the leafhopper Empoasca vitis incooler winegrowing regions (16). However, other authors (117) have come to different conclusions,and pest pressure might also be reduced as a result of the advance in harvest dates that will limitdamage from later pest generations (24).

THE FUTURE FOR VINEYARD PEST MANAGEMENT

Reducing the economic impact of new pest species to viticulture, as with other crop systems,requires more than coordinated programs to address both short- and long-term research needs.Research must be integrated with education programs for growers and their advisors to help im-plement best management practices. The trend toward fewer independent advisors has made thisintegration challenging (103), but modern connectivity now allows greater potential for informa-tion sharing from regions where pests are established to newly invaded regions (80). The examplesprovided above, notably the successful eradication of L. botrana in California, demonstrate thatinternational cooperation is essential for rapid implementation of effective pest management pro-grams. As the distribution of pests continues to spread over long time spans through global warm-ing or rapidly through long-distance movement into new regions, high-quality, research-basedinformation to guide rapid responses to new invasions will be essential to maintain the global sus-tainability of viticulture, and we list here some of the key research areas that should be considered.

Invasive Species Responses

Technological advances over the past decade provide unparalleled opportunity for informationexchange. High-quality photographs and videos can be shared, and large teams of people with adiversity of technical skills can be assembled to communicate about a new pest challenge. Thepower of social media can also be used to raise awareness and gain a network of additional scoutswho can help delimit the distribution of a new invasion. Such networks may also help identifya new pest early in its invasion, improving the chance that effective control programs will beimplemented in time to prevent widespread damage.

Invasive Pest Challenges to Sustainability Programs

Most vineyard sustainability programs employ defined targets that growers must meet to gaincertification. These include lower dependence on insecticides and restrictions on their use. Theappearance of invasive pests or insect-vectored pathogens in production regions can severelychallenge the ability to maintain certification, so short-term exemptions may be built into theprogram’s design. Still, some regions are highly committed to adoption of sustainable practices, asemphasized by the Sonoma County wine grape region in California announcing plans to becomea 100% sustainable production region by 2019 (28).

Molecular Identification of Novel Pests

There are many examples of when a delay in the identification of an invasive pest enabled itsgeographic spread. A global effort could be made to list, photograph, and genetically sequence


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vineyard herbivores so that new finds could be rapidly identified. Pest management programs,including eradication, for known pests could then be more rapidly employed using proven con-trol tools. To support sustainability programs, investigations of their natural enemies could alsoproceed more quickly.

Training/Higher Education

To maintain sustainable viticulture practices, it is essential that trained staff are available to advisegrowers about their pest management needs. Extension educators, private consultants, or vineyardstaff can be vigilant for detection of new pest challenges, and modern communication tools make itmuch easier to transmit photographs of potential new pests to national and international experts.Still, given the trend toward greater invasive pest challenges at the same time that there are oftenfewer agricultural extension staff (103), there remains a significant need for online resources tosupport rapid response to new pest detections.

Adapting to Climate Change

To mitigate pest problems exacerbated by climate change, insight can be gained from the generalrules of direct impact of temperature elevation on insect phenology, life cycles, and distribution(8) and from the few case studies concerning viticultural pests. Predicting future pest distributionbased on single-species studies may be unrealistic as spatial patterns are, at least partly, determinedby interspecific interactions. Indeed, the effect of higher temperatures on the overall abundance ofherbivorous insects remains unknown in the absence of equivalent data on the responses of theirnatural enemies (132).

SUMMARY POINTS

1. Grape production has grown tremendously worldwide and has become a global industrypromoting the movement of both plant materials and invasive pests. That growth hasbeen accompanied by challenges, including entomological challenges.

2. Knowledge of both grape production and pest and natural enemy biology has led toimproved and novel sustainable viticulture programs.

3. The shared development of control programs has enhanced pest management systemsand been essential for the identification, suppression, and/or eradication of invasive pests,as illustrated by the case of Lobesia botrana in California.

4. Climate change, increases in grape production and trade, and the growth of new viticul-tural regions such as China will further challenge entomologists.

FUTURE ISSUES

1. Globally accepted rules for sustainable viticulture will facilitate greater grower adoptionand consumer recognition of these programs.

2. Improved identification and monitoring programs for a greater range of grape pests areneeded.

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3. Global climate change will shift not only wine production regions but also pest populationdynamics.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

Funding that helped to develop this review was provided by Consolidated Central Valley TableGrape Pest and Disease Control District to K.M.D.; we thank Houston Wilson for reviewing anearlier draft and Roxanne Broadway for shared data.

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157. Zangheri S, Donadini P. 1980. Comparsa nel Veneto di un omottero neartico: Metcalfa pruinosa Say(Homoptera, Flatidae). Redia 63:301–05

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http://www.annualreviews.org/r/nevs

EN63-FrontMatter ARI 18 December 2017 14:29

Annual Review ofEntomology

Volume 63, 2018 Contents

The Evolution and Metamorphosis of Arthropod Proteomics andGenomicsJudith H. Willis � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Gustatory Processing in Drosophila melanogasterKristin Scott � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �15

How Many Species of Insects and Other Terrestrial Arthropods AreThere on Earth?Nigel E. Stork � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �31

Pseudacteon Phorid Flies: Host Specificity and Impacts on Solenopsis FireAntsLi Chen and Henry Y. Fadamiro � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �47

Sleep in InsectsCharlotte Helfrich-Forster � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �69

The Discovery of Arthropod-Specific Viruses in HematophagousArthropods: An Open Door to Understanding the Mechanisms ofArbovirus and Arthropod Evolution?Charles H. Calisher and Stephen Higgs � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �87

Social Immunity: Emergence and Evolution of Colony-Level DiseaseProtectionSylvia Cremer, Christopher D. Pull, and Matthias A. Furst � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 105

Neonicotinoids and Other Insect Nicotinic Receptor CompetitiveModulators: Progress and ProspectsJohn E. Casida � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 125

Mosquito Immunobiology: The Intersection of Vector Health and VectorCompetenceLyric C. Bartholomay and Kristin Michel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 145

Insect-Borne Plant Pathogens and Their Vectors: Ecology, Evolution,and Complex InteractionsSanford D. Eigenbrode, Nilsa A. Bosque-Perez, and Thomas S. Davis � � � � � � � � � � � � � � � � � � 169

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Entomological Opportunities and Challenges for Sustainable Viticulturein a Global MarketKent M. Daane, Charles Vincent, Rufus Isaacs, and Claudio Ioriatti � � � � � � � � � � � � � � � � � � � � 193

The Management of Insect Pests in Australian Cotton: An Evolving StoryLewis J. Wilson, Mary E. A. Whitehouse, and Grant A. Herron � � � � � � � � � � � � � � � � � � � � � � � � 215

Ecology, Worldwide Spread, and Management of the Invasive SouthAmerican Tomato Pinworm, Tuta absoluta: Past, Present, and FutureAntonio Biondi, Raul Narciso C. Guedes, Fang-Hao Wan, and Nicolas Desneux � � � � � � � 239

The Psychology of Superorganisms: Collective Decision Making byInsect SocietiesTakao Sasaki and Stephen C. Pratt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 259

Anthropogenic Impacts on Mortality and Population Viability of theMonarch ButterflyStephen B. Malcolm � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 277

Functional Hypoxia in Insects: Definition, Assessment, and Consequencesfor Physiology, Ecology, and EvolutionJon F. Harrison, Kendra J. Greenlee, and Wilco C.E.P. Verberk � � � � � � � � � � � � � � � � � � � � � � � � 303

Nutritional Physiology and Ecology of Honey BeesGeraldine A. Wright, Susan W. Nicolson, and Sharoni Shafir � � � � � � � � � � � � � � � � � � � � � � � � � � 327

Environmental Adaptations, Ecological Filtering, and Dispersal Centralto Insect InvasionsDavid Renault, Mathieu Laparie, Shannon J. McCauley, and Dries Bonte � � � � � � � � � � � � � 345

Alien Invasion: Biology of Philornis Flies Highlighting Philornis downsi, anIntroduced Parasite of Galapagos BirdsSabrina M. McNew and Dale H. Clayton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 369

Systematics, Biology, and Evolution of Microgastrine Parasitoid WaspsJames B. Whitfield, Andrew D. Austin, and Jose L. Fernandez-Triana � � � � � � � � � � � � � � � � 389

Management of Western North American Bark Beetles withSemiochemicalsSteven J. Seybold, Barbara J. Bentz, Christopher J. Fettig, John E. Lundquist,

Robert A. Progar, and Nancy E. Gillette � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 407

Tritrophic Interactions Mediated by Herbivore-Induced Plant Volatiles:Mechanisms, Ecological Relevance, and Application PotentialTed C.J. Turlings and Matthias Erb � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 433

Advances in Attract-and-Kill for Agricultural Pests: Beyond PheromonesPeter C. Gregg, Alice P. Del Socorro, and Peter J. Landolt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 453

Neuroparasitology of Parasite–Insect AssociationsDavid P. Hughes and Frederic Libersat � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 471

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Regulatory Pathways Controlling Female Insect ReproductionSourav Roy, Tusar T. Saha, Zhen Zou, and Alexander S. Raikhel � � � � � � � � � � � � � � � � � � � � � � 489

Entomological Collections in the Age of Big DataAndrew Edward Z. Short, Torsten Dikow, and Corrie S. Moreau � � � � � � � � � � � � � � � � � � � � � � � 513

Phylogeny and Evolution of Neuropterida: Where Have Wings of LaceTaken Us?Michael S. Engel, Shaun L. Winterton, and Laura C.V. Breitkreuz � � � � � � � � � � � � � � � � � � � � 531

Health Hazards Associated with Arthropod Infestation of Stored ProductsJan Hubert, Vaclav Stejskal, Christos G. Athanassiou, and James E. Throne � � � � � � � � � � � 553

Correlates and Consequences of Worker Polymorphism in AntsBill D. Wills, Scott Powell, Michael D. Rivera, and Andrew V. Suarez � � � � � � � � � � � � � � � � � 575

Impact of the Invasive Brown Marmorated Stink Bug in North Americaand Europe: History, Biology, Ecology, and ManagementTracy C. Leskey and Anne L. Nielsen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 599

Indexes

Cumulative Index of Contributing Authors, Volumes 54–63 � � � � � � � � � � � � � � � � � � � � � � � � � � � 619

Cumulative Index of Article Titles, Volumes 54–63 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 625

Errata

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

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