Advancing Vineyard Health: Insights and Innovations for Combating Grapevine Red Blotch and Leafroll Diseases (2025)
Chapter: 5 Research and Actions That May Yield the Most Promising Management Solutions
5
Research and Actions That May Yield the Most Promising Management Solutions
The preceding chapters present the current state of knowledge on the grapevine leafroll-associated virus 3 (GLRaV-3) and grapevine red blotch virus (GRBV) pathosystems, as well as the significant knowledge gaps that remain in understanding these pathosystems. This chapter addresses current management approaches along with areas for future research that could enhance the management of these diseases and the sustainability of viticulture in California. Where appropriate, recommendations are provided to help guide research priorities and approaches to advance management strategies for different sectors of the industry.
Recognizing that the industry needs both short-term and long-term management solutions to these diseases, the committee sought to identify opportunities to improve “stopgap” (i.e., interim) measures to sustain the industry in the near term as research efforts make progress toward elucidating longer-term solutions. In addition, the committee considered how grower perceptions and knowledge of these diseases and their management may impact the adoption of different management practices. There is significant variation in the prevalence of grapevine leafroll disease (GLD) and grapevine red blotch disease (GRBD) among wine grape production regions of California. Likewise, current management practices vary among regions, as well as among growers within regions. For regions where both diseases are established, growers may or may not fully appreciate the differences in each pathosystem in terms of vector ecology and behavior, and although the pathosystems are substantially different, current management practices often share certain general similarities. Because GRBV is a more recent emerging pathogen, less research has been conducted on its management
compared with GLRaV-3, and according to Hobbs et al. (2022), the lack of information and education regarding GRBD has likely impeded the adoption of appropriate management practices. All of this underscores the urgent need to generate and effectively disseminate knowledge about each of these viral diseases and strategies for managing them.
This chapter also addresses the importance of integrating management programs for GLD, GRBD, and other pest issues and vector-borne diseases in California vineyards so that new approaches for the management of one pest do not disrupt the management of others. In this vein, it is encouraging that the California wine grape industry currently employs an array of tactics to mitigate disease spread, especially for GLD (Farrar et al., 2016). Given that all management practices have their own unique pros and cons with regard to development and implementation, the committee attempted to identify the strengths as well as the potential weaknesses or downsides of each strategy so that the industry can make informed decisions about pathways forward.
While the committee believes that all the recommendations in this chapter are important, it is also cognizant of the fact that research funds are limited. Therefore, the committee identified research areas it considers high priority (labeled HP) and medium priority (labeled MP). These research areas are also presented in Table 5-1, at the end of this chapter.
CLEAN PLANTS
Since viruses can spread via clonal propagation of grapevines (both scion cultivars and rootstocks), using “clean” planting material is the first line of defense in establishing healthy vineyards. The National Clean Plant Network (NCPN)1 supports grape clean plant centers in California, Washington State, Missouri, New York, North Carolina, and Florida that maintain foundation collections (i.e., Generation 1 or G1 planting stock) utilizing standard operating diagnostic and pathogen elimination protocols to ensure that plants are free of economically important viruses. These clean plant centers maintain the G1 grapevines on a long-term basis under conditions that mitigate the risk of infection. As an example of the high level of emphasis placed on ensuring the quality and safety of this G1 material, Foundation Plant Services at the University of California, Davis, recently began the process of moving its core foundation collection from an open-field vineyard into a greenhouse environment to further protect it from potential sources of infection.
Commercial nurseries use G1 stock to propagate mother blocks of G2 grapevines, which can be certified and registered under state grapevine
___________________
certification programs. Grapevines propagated directly from registered G2 blocks are then amplified as G3 and G4 vines and supplied as certified stock to growers for planting new vineyards (see Figure 5-1).
At each stage along the supply chain for grapevine planting materials, grapevines (both scions and rootstocks) may be inspected and tested for economically important viruses. As mother blocks represent the transition point between foundation collections and the broader distribution of grapevine stock, ensuring that registered mother blocks remain free of diseases and harmful viruses is especially critical to strengthening clean planting material supply chains, meeting state certification and quarantine criteria, and maintaining growers’ confidence in the value of using clean stock for planting new vineyards. Toward this goal, it is vital to employ robust sampling strategies and state-of-the-art, sensitive, and reliable diagnostic methods (see Box 5-1) to test grapevines in registered mother blocks for
SOURCE: Naidu Rayapati, Washington State University.
BOX 5-1
State-of-the-Art Practices: Key Elements for Reliable Grapevine Virus Detection
Accurate detection of GLRaV-3 and GRBV relies on robust protocols that minimize the risk of false positives and negatives. Both polymerase chain reaction (PCR)-based and high-throughput sequencing (HTS)-based detection methods have specific requirements to ensure diagnostic reliability. Recent advancements, including the development of assays to detect genetically diverse GLRaV-3 variants and the refinement of HTS protocols, have significantly enhanced the accuracy of grapevine virus detection. Below are key elements to consider in developing testing protocols; for more detailed information, refer to the cited publications and the American Phytopathological Society’s Diagnostic Assay Validation Network (DAVN).a DAVN offers tools, a community of practice, and knowledge resources to support the development, implementation, and understanding of validated diagnostic assays for plant pathogens. Adhering to these practices can optimize PCR and HTS methods to deliver reliable and accurate detection of grapevine viruses and reduce the likelihood of diagnostic errors.
PCR-Based Detection Protocols
PCR-based methods, such as reverse-transcription PCR (RT-PCR) and quantitative PCR (qPCR), are well established for detecting specific viruses but require careful attention to several factors to avoid inaccuracies.
Specificity and sensitivity: Design virus-specific primers that target conserved regions to ensure both specificity and sensitivity for the virus of interest and its associated variants. For instance, an available RT-qPCR assay has been shown to detect all known GLRaV-3 variants, including highly divergent ones, by targeting a conserved region in the 3′ untranslated terminal region of the virus genome (Diaz-Lara et al., 2018). As new GLRaV-3 variants emerge, it is important to reevaluate the assay periodically to encompass current knowledge on the genetic diversity of the virus.
Sample quality: Ensure high-quality RNA/DNA extraction to avoid degradation, which could lead to false negatives. The success of PCR-based detection is highly dependent on the quality of the extracted nucleic acids and the sampling time (Chooi et al., 2013; Setiono et al., 2018).
Control use: Incorporate positive and negative controls in each run to validate the results and identify potential contamination or errors (Chooi et al., 2013).
Reaction conditions: Optimize PCR conditions (e.g., annealing temperature, cycle number) to prevent non-specific amplification, which could result in false
positives (Ruiz-Villalba et al., 2017). The use of internal and external references in qPCR assays further enhances assay robustness (Setiono et al., 2018).
Confirmation: Validate positive results with sequencing or additional independent tests to confirm the presence or absence of the virus.
HTS-Based Detection Protocols
HTS-based protocols provide a comprehensive approach to virus detection but require meticulous validation, appropriate controls for each step, and analysis to prevent false results.
Sample preparation and integrity: Maintain high-quality sample processing to ensure that RNA integrity is preserved, which is critical for reliable sequencing outcomes (Hamim et al., 2022).
Bioinformatics analysis and sensitivity: Use rigorous bioinformatics pipelines to accurately assemble and align sequences, and implement contamination monitoring tools (e.g., alien controls) to avoid misinterpretation of data (Massart et al., 2022; Rong et al., 2023). The introduction of new protocols, such as combining petiole and cane sampling across seasons, has been shown to increase the sensitivity of HTS to 100 percent (Soltani et al., 2021).
Controls and thresholds: Apply external controls and set appropriate detection thresholds to distinguish true viral sequences from noise or contaminants (PM 7/151 [1], 2022). The false virus discovery rate should be minimized to reduce the likelihood of false positives, as shown in recent validation studies (Massart et al., 2022).
Expert evaluation: Rely on expert judgment in interpreting results, especially in cases where new or unexpected viruses are detected (Rong et al., 2023). HTS data often require careful interpretation due to the complexity of viral populations within a sample (Javaran et al., 2023).
Validation: Cross-verify HTS findings with traditional methods such as RT-PCR and Sanger sequencing to confirm results and rule out false positives or negatives (Rong et al., 2023). Consistent performance metrics, such as high sensitivity and reproducibility, are essential for HTS to be adopted in routine diagnostics (Massart et al., 2022).
__________________
harmful viruses. It is not sufficient to rely on symptom-based scouting of grapevine nursery materials, since symptoms can be similar for GLD and GRBD and symptoms for both diseases can vary among different cultivars. Instead, reliable diagnostic methods should be employed and samples from a few wine grape cultivars and rootstocks should periodically be subjected to high-throughput sequencing (HTS) to validate diagnostic results.
Productive collaborations between grape clean plant centers, state certification programs and departments of agriculture, certified nurseries, growers, and the broader wine grape industry are vital for nurturing the long-term economic prosperity of the grape and wine industry, while gaps can lead to missed opportunities and undermine the health of the industry. One potential gap is that testing laboratories may not always be providing reliable results to growers and nurseries. In particular, a major concern is whether laboratories testing for GLRaVs are using the most up-to-date testing protocols to keep pace with the rapid evolution of the viruses (Maree et al., 2015; Li et al., 2022). The University of California, Davis, Foundation Plant Services (FPS) Center devotes considerable effort to optimizing detection and identification protocols; encouraging commercial testing labs to adopt standard protocols could decrease the risk of false negatives going forward. To ensure that appropriate protocols are used, industry members could take the position of only using labs that employ “FPS-validated” protocols for testing (e.g., Protocol 2010).2 In the context of large-scale testing, it is ideal to employ affordable diagnostic tests that accurately detect the widest range of genetic variants; for example, the California Department of Food and Agriculture uses enzyme-linked immunosorbent assay (ELISA), an approach that is also aligned with Protocol 2010 recommendations, for testing in the California Registration and Certification Program for Grapevines (Li et al., 2022).
A second concern is that commercial testing laboratories in California are largely unregulated in their technical standards, and there have been reports of inconsistencies in diagnostic results across laboratories.3 This variation in laboratory results could arise from not using standard assays, as discussed above, or from a lack of proper training, technique, or equipment. A certification scheme for testing laboratories would help ensure that different laboratories are using best practices and up-to-date diagnostics for virus detection. Such certification programs for laboratory standards already exist in other agricultural arenas. For example, the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service oversees accreditation programs for detection of sudden oak death
___________________
2 See https://fps.ucdavis.edu/fgr2010.cfm.
3 This concern was mentioned by a grower association representative at the committee’s open meeting at the University of California, Davis, on March 5, 2024.
(caused by Phytophthora ramorum) and citrus greening (also known as Huanglongbing, or HLB, caused by Candidatus Liberibacter asiaticus).4 An alternative to government oversight is industry-driven accreditation, as exemplified by an industry group5 that provides certification for plant and soil nutrient analyses. The industry may consider developing an industry-driven ring-test process with the assistance of FPS to help assure that laboratories are providing valid results with the most up-to-date assay protocols (Cardwell et al., 2018). Whatever model is used, providing greater assurance in the reliability and accuracy of testing would benefit efforts to detect and manage these grapevine diseases, both for ensuring that new planting materials are disease-free and for informing management strategies once viruses are present in a vineyard. Since the cost of commercial testing may also be an impediment for growers, a more standardized approach could also potentially help bring costs down or at least offer reassurance of the quality of diagnostic results and thereby encourage greater use of testing to inform management tactics such as rouging virus-positive tested vines (Speirs et al., 2013).
Conclusion 5-1: Using clean planting material is the first line of defense in establishing healthy vineyards because viruses can spread via clonal propagation of grapevines.
Conclusion 5-2: There are concerns regarding the reliability of results from testing laboratories; these stem from questions about whether testing for GLRaVs and GRBV is being done using the most up-to-date protocols to detect all variants, and from the fact that commercial testing laboratories are largely unregulated in their technical standards, potentially resulting in inconsistencies in diagnostic results across laboratories.
Recommendation 5-1 (HP): Encourage the adoption and implementation of higher sanitary standards in registered mother blocks using robust, state-of-the-art, sensitive, and reliable diagnostic methods and roguing of infected vines to maintain disease-free stock and provide clean planting materials for growers.
This could include engaging FPS in exploring the potential of developing a ring-test process or similar validation scheme to better assure the validity and reliability of diagnostics from laboratories working with the industry.
___________________
4 See https://www.aphis.usda.gov/plant-pests-diseases/citrus-diseases/citrus-greening.
5 See https://alta.ag/about.
ROGUING INFECTED VINES
Grape growers may employ roguing to reduce the spread of viruses within vineyards. Roguing during the first years after establishment of a block of vines has proven effective in reducing and even eliminating GLD in individual vineyards (Almeida et al., 2013; Pietersen et al., 2013; Ricketts et al., 2015). In South Africa, roguing when the incidence of GLRaV-3 is below 20 percent is recommended as part of the GLD integrated management program, which also includes planting clean vines and management of the vector (mealybug) using systemic insecticides and biological control. This strategy has nearly eliminated GLRaV-3 from South African vineyards that produce high-end wines (Pietersen, 2024). However, the threshold for deciding when roguing is cost-effective rests on assumptions that may not be valid (Pietersen et al., 2013). Consequently, it is essential to evaluate this threshold to improve the adoption rate of roguing as a management strategy.
Optimal roguing schemes may be different for different production regions in California, which vary widely with regard to their market economics and the environmental conditions that affect vector and virus dynamics (Ricketts et al., 2017). Cunniffe et al. (2022) present a framework for modeling complex interactions among viruses, vectors, and plants. This framework aims to better characterize disease spread and identify key points in the process for targeted management. Implementing such a framework could enhance decision making in viral disease management. However, refining roguing schemes requires addressing some important knowledge gaps. For example, mealybugs, which transmit GLRaVs, are known to move on a local “plant to plant” scale as well as by long-range passive dispersal, while movement patterns of the three-cornered alfalfa hopper (TCAH) and the spread of GRBV are not as well characterized (see TCAH Host Preference and Movement Dynamics section in Chapter 4). Knowledge gaps regarding TCAH flight behavior and the impact and behavior of other potential GRBV vectors substantially impair the development of roguing schemes and other management practices in the context of GRBD. Limited information from Oregon indicates that roguing can mitigate the spread of GRBD (Achala et al., 2022), but the abundance of TCAH in that area is unknown. The relative importance of the primary versus secondary spread of GRBV is also unclear. In addition to determining when roguing is the best management choice and which vines should be rogued, there is also a need to define methods for vine removal that minimize the risk of re-infection. In the case of GLD, leaving root systems of rogued vines in the vineyard has been shown to create a reservoir for GLRaV-3 and mealybugs that can develop within the remnant root systems and continue to spread the virus (Bell et al., 2009).
Implementing roguing and replanting can be difficult for growers to justify because infected grapevines can still be productive whereas replanted vines are not immediately productive. Also, the effectiveness of roguing and replanting may be impacted by the abundance of virus inoculum and vectors within the surrounding landscape. This points to a critical need for economic analysis on the cost-effectiveness of roguing and replanting schemes (Sisterson and Stenger, 2012). Modeling efforts have shown that as vector density and dispersal increase, roguing individual vines for GLD becomes less effective in suppressing disease spread, and economically may be less cost-effective than replanting entire vineyard blocks (Mannini and Digiaro, 2017; Bell et al., 2021). Less information is available for developing roguing schemes for GRBD. Aside from the expense, roguing and replanting can also complicate viticultural practices, as having vines at different stages (such as when younger vines are replanted into older blocks) or having gaps where vines are simply rogued and not replaced can require adjustments to management practices within a vineyard (Ricketts et al., 2015; Mannini and Digiaro, 2017).
Conclusion 5-3: Roguing has been shown to be effective in GLD management and in mitigating GRBD spread, but it can be difficult for growers to justify removing infected but still productive vines and replacing them with new vines that will not immediately bear fruits. Both roguing and roguing followed by replanting also complicate viticultural practices in vineyards.
Conclusion 5-4: There is insufficient information available for developing effective roguing schemes for GLD and GRBD. Specifically, more data are needed on the determination of threshold decision points, the cost-effectiveness of roguing under various conditions, and the influence of movement patterns and flight behavior of TCAH and other potential GRBV vectors on the spread of GRBD.
Conclusion 5-5: Roguing schemes need to be optimized for California production regions in light of differences in market economics and in the environmental conditions that affect vector and virus dynamics. Additional epidemiological research may reveal the optimum roguing and replanting schemes for both GLD and GRBD in different production regions and for vineyards with differing business models.
Recommendation 5-2 (HP): Support research to develop optimal roguing and replanting schemes and techniques to manage GLD and GRBD and to facilitate their implementation by growers.
This could include studies to determine:
- The cost-effectiveness of roguing and/or replanting based on disease incidence and rate of spread.
- How long it typically takes for newly planted clean grapevines to become infected and become sources of inoculum.
- Best practices for removal of remnant root systems of rogued vines to prevent them from serving as reservoirs for the vector and virus.
- Roguing schemes suited to the different grape production regions in California.
VECTOR MANAGEMENT
Because of the inherent complexities of the GLD and GRBD pathosystems, no single tactic is likely to provide a complete and sustainable management solution. To maximize the benefits of clean plant programs, the use of clean plants and roguing schemes needs to be complemented by effective strategies for managing the vectors that carry viruses into and within vineyards (Daane and Haviland, 2024). Vector management is expected to have even greater importance in the future, as climate warming is likely to exacerbate mealybug populations. Higher temperatures will allow additional mealybug generations to develop, and rising temperatures may also increase protective behaviors in mealybug-tending ants (Zhou et al., 2017). Overall, increasing temperatures have been predicted to lead to increased mealybug populations and decreasing efficacy of their natural enemies because of greater asynchrony in the temporal and spatial distributions of populations (Gutierrez et al., 2008). Increasing temperatures will also affect the phenology of TCAH hosts in and around vineyards and the development of the treehopper, which could lead to earlier dispersal into vineyards and larger populations (Jordan, 1952; Preto et al., 2019; Bick et al., 2020).
Monitoring vector populations is fundamental to successful vector management. Information from monitoring programs not only allows growers to determine when to employ pest management measures but also to evaluate their effectiveness. The University of California’s guidelines for grape pest management6 include well-developed resources for implementing monitoring programs for mealybugs and scales. Sex pheromones that can be employed in monitoring efforts are commercially available for certain mealybugs, including the vine mealybug (Millar et al., 2002). For monitoring TCAH in vineyards, both sweep net sampling and yellow sticky traps have been used effectively (Wilson et al., n.d.), although sweep net sampling
___________________
has been found to provide a more accurate estimate of adult populations and sex ratios than sticky card trapping (Johnson and Mueller, 1990).
Any consideration of the use of insecticides for vector management must include careful attention to optimizing the insecticide type and application strategy used. It is also important to consider the policy context for insecticide use, which may affect the types of products or practices that will be allowable in the future. In 2023, the California Department of Pesticide Regulation published the “Accelerating Sustainable Pest Management: A Roadmap for California,” which outlines a goal of identifying and eliminating the use of certain “Priority Pesticides” (defined based on hazards to human and ecosystem health) by 2050 (CDPR, 2023). Awareness of pesticides that may eventually be phased out under this initiative can help to inform where research investments focused on insecticides for GLD and GRBV vectors are likely to be most impactful in the long run.
Insecticides for Mealybug Management
Insecticides can be effective for mealybug management; however, insecticides alone will not stop the spread of GLD and should be considered a complementary approach to be combined with other tactics. In addition, only certain types of insecticides are likely to be effective. The tendency for mealybugs to aggregate in concealed areas can reduce their exposure to contact insecticides. Systemic insecticides such as neonicotinoids and spirotetramat, which move in the plant phloem and xylem, offer better management options. Because systemic insecticides can move to enclosed areas of plants, they can reach mealybugs in concealed areas; they also tend to have relatively long residual activity in plants (Van Timmeren et al., 2012). However, systemic insecticides require insects to feed in order to ingest the toxins. Given that mealybugs can transmit GLRaVs in a short period of time (about 1 hour) (Tsai et al., 2008), systemic insecticides would not likely disrupt feeding quickly enough to stop virus transmission. Therefore, the value of these insecticides lies in overall population suppression (O’Hearn and Walsh, 2020).
Increasing the transport of the active ingredients of systemic insecticides throughout vine tissues and increasing their longevity in the plant could further improve the effectiveness of these insecticides for mealybug management. For example, spirotetramat must be metabolized in the plant to spirotetramat-enol, which is the toxin that kills immature mealybugs and can reduce adult fecundity. Since the conversion efficiency to the enol metabolite depends on environmental factors and physiological conditions of the plant (Martin, 2021), variation in these conditions can result in differences in the amount of toxin present in leaf samples after an application. Within-plant distribution of the toxin also may not be uniform, allowing
mealybugs in areas such as the trunks to be more likely to escape exposure or to be exposed to lower doses. Environmental conditions can also influence the efficacy of systemic insecticides. For example, soil type affects neonicotinoid activity; imidacloprid has greater efficacy in lighter, sandier soils, whereas thiamethoxam has greater efficacy in heavier loam and clay soils (Kurwadkar et al., 2013). This suggests that the local environmental conditions are an important consideration to guide insecticide selection.
The strategy and timing of delivery for insecticides also influences their effectiveness. Delivering therapeutics at the right time and in the right amount to woody plant vasculature is a challenge for controlling insect vectors in many pathosystems. One way to overcome this is to consider the use of unconventional pesticide delivery methods such as trunk injection (see Trunk Injection of Systemic Pesticides section in Chapter 6). In addition, because of the broad use of insecticides such as neonicotinoids in grapevines for multiple pests, determining the optimal timing for insecticide sprays is critical to maximize efficacy and avoid ineffective and unnecessary applications (Hamby et al., 2015; Mermer et al., 2021). For example, applications of contact insecticides targeting mealybug crawlers would be ineffective if they are made when crawlers are not active.
Finally, the reliance on a limited number of insecticides with similar mode of action predisposes the grape industry to the development of insecticide resistance (Venkatesan et al., 2016). Spirotetramat has been widely used over the past decade with growers anecdotally reporting decreasing efficacy. Likewise, the widespread use of imidacloprid for glassy-winged sharpshooter management could contribute to the evolution of resistance to this pesticide in mealybugs and TCAH. As such, there is a critical need for implementing insecticide resistance management programs and for the development of new active ingredients for vector management. Venkatesan et al. (2016) provide recommendations for resistance management. There has been progress in identifying more selective insecticides for mealybug management and more effective products for organic production (Poliakon et al., 2017; Tacoli et al., 2018; Deza-Borau et al., 2020). Other natural products, such as plant essential oils, have potential to cause significant mortality (Tacoli et al., 2018).
Conclusion 5-6: Contact insecticides are not effective in controlling mealybugs due to the cryptic nature of mealybug behavior. Systemic insecticides will not likely disrupt feeding quickly enough to stop transmission of GLRaVs, but they could be effective in reducing mealybug populations. In addition to their crypsis, the sessile nature of mealybugs suggests that systemic insecticides, even if slow acting, could reduce secondary spread of GLRaV-3. Primary spread from mealybugs entering vineyards would require a more rapid kill time.
Conclusion 5-7: Knowledge of factors that affect the efficacy of insecticides (e.g., physiology of the plant, environmental conditions, soil type, insect behavior, insecticide application method) is important in developing improved guidelines for their application.
Conclusion 5-8: Reliance on a small set of insecticides for mealybug control increases the likelihood that mealybugs will develop resistance to them.
Recommendation 5-3 (HP): Support research to determine the optimal conditions for the application of systemic insecticides to achieve better mealybug control.
Recommendation 5-4 (HP): Develop and implement insecticide resistance management programs and support research to develop new active ingredients for mealybug management, including by evaluating the efficacy of natural products, such as plant essential oils, that could provide additional options for both organic and conventional vineyards.
Insecticides for TCAH Management
Insecticide application could play an important role in TCAH management, but more information is needed to assess the pros and cons and ensure the effectiveness of this tactic. In particular, it will be important to have a better understanding of virus transmission dynamics. Although secondary spread of GRBV (between vines within an already-infected vineyard) has been documented, the relative importance of primary spread (introduction into a previously uninfected vineyard from outside the vineyard) versus secondary spread is unknown (Cieniewicz et al., 2019). Insecticide control is rarely successful in preventing primary spread, whereas insecticides may be effective in limiting secondary spread (Perring et al., 1999), so clarifying the relative importance of primary versus secondary spread in the context of GRBV could help to guide decisions about insecticide use.
A better understanding of virus-vector dynamics is also needed. TCAH appears to be transient in grapevines, and insecticides are not effective in controlling primary disease spread from transient vectors with a short inoculation time of nonpersistent pathogens (Perring et al., 1999). Systemic insecticides, such as neonicotinoids, require the insect to feed on treated plants to acquire a lethal dose of the insecticide, which generally makes them ineffective for managing pathogens requiring brief inoculation times (Almeida et al., 2013). However, certain systemic insecticides may interfere with feeding by hemipteran vectors, which can reduce the transmission
of plant viruses by individual vectors (Garzo et al., 2020). Beyer et al. (2017) reviewed the insecticide recommendations for TCAH in annual crops (peanut, soybean) and perennial forages (alfalfa) and found that most of the products listed are broad-spectrum insecticides, such as pyrethroids, carbamates, and neonicotinoids. In their review of insecticide treatments against TCAH on soybeans, alfalfa, and peanuts, Bradley and Kuhar (2023) noted that flupyradifurone (Sivanto), a Group 4D butanolide, was highly efficacious. The circulative transmission mode and lengthy inoculation access period of GRBV by the TCAH suggests that insecticide applications have the potential to be effective, as has been demonstrated for other circulatively transmitted pathogens (Garzo et al., 2020). In addition, because transmission of GRBV appears to require a long feeding time for acquisition, there is potential to develop a decision support system based on diagnosing the abundance of viruliferous TCAH in a region to guide the timing of insecticide applications, if warranted (Stillson et al., 2020).
Should insecticide use become a broadly implemented technique for GRBV management, insecticide resistance monitoring would become important and regional testing for insecticide susceptibility among populations of TCAH would provide critical baseline data and help to minimize the risks of insecticide failures (Roush and Miller, 1986; Prabhaker et al., 2006). In addition, since wine grapes are subject to damage from a range of pests, any insecticide use must take into account the effects of insecticides on both target pests and non-target insects. For example, some of the insecticides identified as candidates for managing TCAH may also be used against mealybugs and the glassy-winged sharpshooter, suggesting that applying them to control TCAH in vineyards could have implications for resistance management where multiple pests occur on one crop. It is also important to recognize that insecticide use can inadvertently exacerbate pest problems. Spinosyn-based insecticides may trigger outbreaks of secondary pests, including planthoppers, because of the elimination of natural enemies of those secondary pests (Duso et al., 2022), while pyrethroids that can be used to target planthoppers may trigger outbreaks of spider mites and other types of planthoppers. These outbreaks can result from hormesis, the phenomenon in which sublethal doses of insecticides promote insect reproduction, as well as the elimination of natural enemies of secondary pests (Trichilo and Wilson, 1993).
Finally, economic or action thresholds for insecticide application to manage the vectors of GLRaVs and GRBV are still lacking. Although there is essentially a zero-mealybug tolerance for wine grapes, it is not known if this standard is appropriate (Daane et al., 2013). The establishment of economic thresholds for management of any vector should be based on a thorough understanding of the epidemiology of the diseases involved (Perring et al., 1999).
Conclusion 5-9: A better understanding of GRBV acquisition and transmission dynamics is needed to improve the effectiveness of insecticide application as a control tactic against TCAH, and appropriate economic or action thresholds are needed to guide insecticide application programs.
Recommendation 5-5 (HP): Support research to determine the optimum conditions for the application of insecticides to achieve better TCAH control and to establish economic or action thresholds to guide insecticide application programs.
Mating Disruption
Mating disruption, a technique that uses artificial stimuli (e.g., synthetic sex pheromone) that confuse individuals and disrupt mate location or courtship behaviors to block the reproductive cycle, has been used for mealybug management in California vineyards for two decades. Currently, sex pheromone for mating disruption is commercially available for the vine mealybug (Planococcus ficus) only. Sex pheromones have been identified for grape mealybugs (Pseudococcus maritimus) (Figadère et al., 2007), obscure mealybugs (Pseudococcus viburni) (Millar et al., 2005), and longtailed mealybugs (Pseudococcus longispinus) (Millar et al., 2009); experiments with the use of sex pheromones for mating disruption are underway for grape mealybugs (Millar et al., 2005; Bahder et al., 2013).
Mating disruption programs have shown clear decreases in vine mealybug populations and damage. To maximize the effectiveness of mating disruption for mealybug control, research findings suggest that it is important to deploy pheromones throughout the growing season and especially during the late season (September and October) when male vine mealybug flights peak (Daane et al., 2020). Research also shows that mating disruption tends to be most effective when it is employed over longer timescales and on larger spatial scales, indicating the benefit of using areawide programs with consistent deployment of pheromones during critical population periods (Sharon et al., 2016; Cocco et al., 2018; Hogg et al., 2021). However, no studies have been undertaken to determine the impact of mealybug mating disruption on GLRaV-3 spread, likely due to barriers from a lack of rapid virus detection methods and funding for long-term studies.
Additional information is needed to improve the efficacy of mating disruption, in particular regarding the appropriate number and type of pheromone dispensers to use to ensure optimal coverage in time and space. Pheromones can be released into the environment through various dispenser types or by direct application of the chemical to an area (Benelli et al., 2019). Researchers have evaluated the efficacy of using passive dispensers
(Cocco et al., 2014; Sharon et al., 2016; Mansour et al., 2017; Lucchi et al., 2019; Daane et al., 2021; Hogg et al., 2021), aerosolized canisters (Benelli et al., 2019; Daane et al., 2021), and flowable microencapsulated formulations (Daane et al., 2021) to release sex pheromones targeting the vine mealybug. Microencapsulated formulations are distinct from other dispersion methods because they are applied in the same manner as other flowable agrochemicals, thereby eliminating some of the logistical and technical constraints of using dispensers to disperse pheromones in vineyards (Daane et al., 2021). All pheromone application methods have been shown to lower densities and/or damage of the vine mealybug, and some show reductions in the first year and following seasons (Cocco et al., 2014; Lucchi et al., 2019; Daane et al., 2020), but lasting results appear to be influenced by location and year (Daane et al., 2021). To further improve efficiency and reduce costs, researchers are examining ways to lower the densities of dispensers and use programmable dispensers to align pheromone dispersion with flight times (Daane et al., 2021).
A better understanding of basic information about mealybug mating behavior, seasonal adult male flight behavior, seasonal sex ratios, and regional differences in the timing of male flights and generation numbers would help to elucidate how and where mating disruption programs will be the most effective. Mealybug females display diel periodicity in the release of pheromones, which affects male activity and the timing of mating (Levi-Zada et al., 2014). Characterization of how environmental and endogenous (e.g., female age) factors may affect pheromone release could be used to improve mating disruption programs (e.g., by informing the timing of pheromone release from puffer devices) (Daane et al., 2020). In addition, having a better understanding of the mechanism by which pheromone releases disrupt mating behavior through either noncompetitive disruption (in which female pheromones are masked by the inundation of synthetic pheromones) or competitive disruption (in which dispensers create false pheromone plumes that males follow instead of following real plumes from females) would also help inform the optimal placement of pheromone dispensers in the field. Competitive and noncompetitive disruption have been studied for lepidopteran pests (Miller et al., 2006; McGhee, 2014; Miller and Gut, 2015); however, the biology and behavior of moths and butterflies is markedly different from mealybugs with regard to location, lifespan, flight capabilities, and other factors, making it difficult to translate these research insights to inform mealybug management. Finally, additional information is needed to guide the timing of pheromone dispersion, including information about generation development, which influences when male flights occur; the establishment of effective in-field or predictive population models of mealybug generation could help guide the timing of mating disruption activities.
Even with improvements in the techniques used, mating disruption is unlikely to completely eliminate vine mealybug populations, suggesting that it should be complemented by additional management tactics such as insecticide application and/or biological control. Long-term studies are needed to assess the persistence of mealybug population suppression using mating disruption, the short- and long-term importance and economics of continued insecticide applications compared with mating disruption, and the optimal timing for applications of insecticides and pheromones when these tactics are used in combination. Since mating disruption works better when mealybug densities are low, the use of insecticides at the start of a mating disruption program may help to reduce populations early and increase the efficacy of mating disruption (Walton et al., 2006; Cocco et al., 2018; Daane et al., 2020; Hogg et al., 2021). Insecticides may also be needed at different time points after the initiation of mating disruption programs in areas where mealybug density is high or rebounds. It would be helpful to further elucidate the efficacy of different flowable pheromone products, to refine thresholds for spraying insecticides in combination with mating disruption, and to understand the dynamics of mealybug suppression beyond a two-year period, especially where low population densities are achieved (Hogg et al., 2021). Results of one study showed that two and three applications of a flowable pheromone formulation reduced vine mealybug populations to the same and a greater extent, respectively, compared with a grower-standard insecticide treatment from June through August in a California wine grape vineyard (Daane et al., 2021). Since the densities of mealybugs on trunks do not always decrease concurrent with trap captures, further studies could also help to refine the frequency of continued management after pheromone trap captures of male mealybugs decrease. In addition, more information is needed about potential synergies between mating disruption programs and biological control (Shapira et al., 2018). Because biological control agents are also more effective at reducing mealybug populations when the pest populations are low, it would be useful to examine whether growers can reap additional pest suppression benefits by complementing mating disruption with biological control (Daane et al., 2012).
Mating disruption via sex pheromones is unlikely to be effective in reducing the spread of GRBV because sex pheromones are unknown among the family Membracidae and do not appear to be part of mating behavior in TCAH (Wood, 1993). However, since hemipteran insects such as TCAH use acoustic signals and substrate-borne vibrations to locate mates (Hunt, 1993), they may be susceptible to acoustic or vibrational disruptions that interfere with mating behavior (Mankin, 2012). Initial research on the disruption of substrate-borne mating vibrations for a leafhopper (Scaphoideus titanus) that vectors the grape phytoplasma Flavescence dorée has been
carried out in Italy. Research has demonstrated that mating in the open field can be disrupted with vibrations generated by a specialized shaker device (Polajnar et al., 2016). However, such a mating disruption system may not be practical for TCAH because mating likely occurs off of grapevines and outside of vineyards (Mitchell and Newson, 1984; Sisterson et al., 2022).
Conclusion 5-10: Mating disruption tends to be most effective in reducing mealybug populations when used over longer timescales and on larger spatial scales. More information is needed to determine the optimum number and type of pheromone dispensers to use to ensure coverage in time and space while reducing the cost of employing this technique.
Conclusion 5-11: Mating disruption has been shown to decrease vine mealybug populations and damage, but no studies have been done to determine the impact of mating disruption on GLRaV-3 spread.
Conclusion 5-12: Knowledge about the mating disruption mechanism in mealybugs (i.e., competitive or noncompetitive) and about mealybug biology, behavior, and generation development could help identify optimal times for dispersing pheromones to disrupt mating. In-field or predictive population models of mealybug generation may also help guide timing of mating disruption activities.
Conclusion 5-13: Studies are needed to determine how long mating disruption can suppress mealybug populations and guide the use, frequency, and timing of insecticide applications to keep mealybug populations low.
Conclusion 5-14: Studies are needed to determine and compare the short- and long-term efficacy and economics of various techniques for applying pheromones in mating disruption programs.
Conclusion 5-15: Studies are needed to inform integrated pest management (IPM) decision making by elucidating the potential impacts of biological control tactics such as leveraging natural enemies alongside mating disruption programs.
Conclusion 5-16: Mating disruption is not likely to be a practical management tactic for TCAH, as leafhoppers do not appear to use long-range sex pheromones to locate mates but instead use substrate-borne vibrational signals that occur off of grapevines.
Recommendation 5-6 (HP): Support research to generate information needed for improving the efficacy of mating disruption for mealybug control and to determine the benefits (economic and otherwise) of employing this technique as part of an integrated approach to manage insect vectors in grapevines.
This could include studies to determine:
- The optimum number and type of pheromone dispensers for ensuring coverage over an extended period over a large area.
- Mealybug mating behavior, seasonal adult male flight behavior, seasonal sex ratios, regional differences in the timing of male flights, generation development, and the mechanism of mating disruption in mealybugs.
- How long mating disruption can suppress mealybug populations and how insecticides and natural enemies can be used to complement mating disruption to keep mealybug populations low.
- The impact of mating disruption on GLRaV-3 spread.
Ultraviolet Light for Mealybug Management
In recent years, the effect of ultraviolet (UV-C) light has been explored as a non-chemical strategy to manage insect populations that cause damage to crops as pests and disease vectors. The use of UV-C has shown promising results as a control measure against common insect pests, such as two-spotted spider mites (Tetranychus urticae Koch), chili thrips (Scirtothrips dorsalis Hood), and western flower thrips (Frankliniella occidentalis Pergande) in strawberries (Montemayor et al., 2023). UV-C applications have also been shown to help combat powdery mildew on strawberries (Onofre et al., 2021) and grapevines (McDaniel et al., 2024b) with no adverse effects on fruit yield and quality. A recent study by McDaniel et al. (2024a) reported potential impacts of UV-C light treatment on grape mealybug nymph mortality, suggesting that UV-C could represent a valuable IPM approach to suppress mealybug populations in vineyards. UV-C applications in vineyards may not be practical for TCAH, however, because these insects do not reside primarily within vineyards.
Conclusion 5-17: Emerging research suggests that the use of UV-C light could help to suppress pest populations without negatively impacting crop yield. However, further refinement of this method is needed to make it an effective tool for vine mealybug management in vineyards.
Recommendation 5-7: Support research to further refine UV-C treatment of grapevines to complement other IPM strategies to suppress field populations of mealybug vectors in vineyards.
CULTURAL CONTROL
Although they are only known to spread GRBV to Vitis species, TCAH spend significant amounts of time on other plants. Cultural control practices such as removal of reproductive hosts or the use of trap crops could offer opportunities for reducing populations of viruliferous TCAH on grapevines.
TCAH appear to favor leguminous plants as reproductive hosts (Kron and Sisterson, 2020). Recent research shows that removal of vegetation between rows of grapevines in the spring may reduce populations of TCAH within vineyards by reducing the availability of such reproductive hosts (Bick et al., 2020; Billings et al., 2021). The complete removal of vegetation by discing at times specified by degree-day modeling has proven to be more effective than mowing (Bick et al., 2020), and Billings et al. (2021) found that discing ground covers in the early spring could reduce the abundance of TCAH in vineyards. All cover crops in this study were mixtures that contained legumes; specific mixtures of ground covers, especially limited to non-leguminous hosts, designed to reduce TCAH were not evaluated, no comparison of cover crop termination methods to clean cultivation were made, and no measures were included to assess changes in the rates of disease spread. Billings et al. (2021) also do not fully address the costs and benefits of ground cover removal. Vegetation removal can increase soil erosion, especially in steep terrains (Xu et al., 2013), and also raises concerns regarding the potential effects on natural enemies of all vineyard pests (Sáenz-Romo et al., 2019), which could adversely affect biological control of both mealybugs and TCAH. Legumes can comprise a large component of weedy vegetation inside and outside vineyards and have certain features that enhance vineyard health; legume cover crops have been used in vineyards as a sustainable means to provide nitrogen to vines (Ovalle et al., 2010), and they may provide floral resources for natural enemies of TCAH and other grape pests. Therefore, large-scale vegetation removal could have important downsides that would need to be weighed against the potential benefits for TCAH management.
Trap crops are defined as plants “that serve to attract, divert, intercept, and/or retain targeted insects or the pathogens they vector in order to reduce damage to the main crop” (Shelton and Badenes-Perez, 2006). While trap cropping has proven beneficial in numerous cropping systems, their utility for the management of TCAH and GRBV is unknown. Trap crops can be employed in different ways to reduce pest populations (Sarkar et al., 2018);
they have been used, but with limited success, with intercropping and border plantings to limit pathogen spread. One of the most notable examples of trap crop use is in reducing infection of potato with potato virus Y, a non-persistently transmitted aphid-borne virus (Dupuis et al., 2017). Trap crops reduce the spread of non-persistently transmitted viruses when the vector encounters them before moving to the main crop. The vector feeds on and transmits the virus to the non-host trap crop, which significantly depletes or eliminates the virus from the vector mouthparts so there is little or no virus transmitted by the time the vector moves into and feeds on the main crop. In the case of GRBV, which persists in the TCAH, this strategy would only be effective if the trap crop is attractive enough to concentrate TCAH and prevent the vector from moving into vineyards before an insecticide can be applied to the trap crop. This strategy has been demonstrated in tarnished plant bugs (Lygus lineolaris) treated with an insecticide while concentrated on a mullein trap crop (Dumont and Provost, 2022). Alfalfa has also been used as a trap crop to reduce colonization of strawberry by L. lineolaris. Since TCAH also has an affinity for alfalfa (Wistrom et al., 2010), alfalfa may have potential as a trap crop for TCAH. More research is needed to better understand TCAH-plant host interactions and assess whether this type of habitat manipulation is a viable strategy for reducing the spread of GRBV. Because the ecology and biology of mealybugs and GLRaVs differ from those of TCAH, the use of trap crops for GLD management would likely be ineffective.
Conclusion 5-18: Removal of vegetation (such as legumes, which serve as reproductive hosts) between rows of grapevines in the spring may reduce populations of TCAH within vineyards, but information about the costs and benefits of this practice is lacking.
Conclusion 5-19: Trap crops have been shown to reduce the spread of non-persistently transmitted viruses, but the feasibility of using trap crops to control GRBV, which is persistently transmitted by TCAH, has not been determined.
Recommendation 5-8 (MP): Support research to determine the costs and benefits of removing vegetation that harbors TCAH in and around vineyards and the use of trap crops to inform grower decision making regarding the employment of these methods for managing TCAH in vineyards.
BIOLOGICAL CONTROL
Biological control strategies can be used to help reduce the population of an insect pest or vector by creating conditions under which that insect will be more vulnerable to the effects of predators, parasites, or other biological agents that threaten its survival or reproduction. Some progress has been made in developing biocontrol strategies for mealybugs; less is known about potential biocontrol strategies for TCAH.
Several parasitoids and predators of the vine mealybug have been identified that may contribute to mealybug control in California. Most IPM programs have emphasized conservation biological control (i.e., minimizing disruptions to naturally occurring populations of natural enemies). However, deliberate releases can also be used; for example, several insectaries produce the parasitoid Anagyrus pseudococci for inundative releases in the spring.7 Releasing this parasitoid before naturally occurring populations typically become active may help to overcome the lag between mealybug population increases and the effective control by parasitoids (Malakar-Kuenen et al., 2001). In addition to parasitoids, several predators have been documented preying on mealybugs in vineyards. These include lady beetles (Coleoptera: Coccinellidae), especially the mealybug destroyer (Cryptolaemus montrouzieri), brown and green lacewings (Neuroptera: Hemerobiidae, Chrysopidae), predatory gall midges (Diptera: Cecidomyiidae), and spiders. However, most mealybug predators are generalists (i.e., they prey on a wide range of small, soft-bodied insects) and information is lacking on their effectiveness as biocontrol agents in vineyards (Daane et al., 2012). In Italy, combined inundative releases of the parasitoid Anagyrus sp. near pseudococci and C. montrouzieri have proven effective in managing P. ficus when insecticides have not been applied against it or other pests (Lucchi and Benelli, 2018).
Entomopathogenic fungi (EPF) offer an additional biocontrol tactic. Numerous species of EPF have been identified that impact vine mealybug, grape mealybug, and other vectors of GLRaVs (Sharma et al., 2018). The successful use of EPFs in biological control is dependent on identifying the most effective strains or isolates to use for a particular pest in a particular crop. Commercial formulations of certain EPFs are available and registered for use in grapes, where they can be used as microbial insecticides for inundative biological control. However, the available formulations require repeated applications to contribute to pest suppression (Fuxa, 1987; Jaronski, 2010), and EPFs in general tend to lose infectivity and virulence under harsh environmental conditions. High temperatures and ultraviolet light, typical of California vineyards during the growing season, tend to
___________________
7 See https://www.countyofnapa.org/DocumentCenter/View/32581.
degrade EPFs. Identification and mitigation of abiotic and biotic factors that degrade EPFs could make it possible to establish self-perpetuating populations of EPFs to provide ongoing suppression of vector populations within vineyards. In addition, previously unidentified EPF strains may be more efficacious than the strains that are currently commercially available, although such novel strains would need to demonstrate appropriate safety with regard to human health when applied to a food crop, as well as environmental safety with regard to impacts on non-target organisms, in order to be approved for use.8 The use of locally obtained strains may facilitate the registration process (Lima, 1992).
The efficacy of biocontrol strategies can be compromised by ants, which tend mealybugs to access the honeydew that the mealybugs excrete. Ants disrupt the natural enemies of mealybugs and also promote mealybug survival and development through other mechanisms (Daane et al., 2007). Parasitism levels of mealybugs are significantly higher in the absence of ants than when ants are present (Daane et al., 2007). In addition to disrupting biological control, certain species of ants may move mealybugs to new locations within or between vines (Daane et al., 2007; Grasswitz and James, 2008). Although this behavior has been observed, the extent to which it may facilitate the dispersal of mealybugs and the development of new mealybug colonies has not been studied and remains unknown.
Bait stations, similar to those used in residences, have been developed to help manage ants in vineyards (Daane et al., 2008; Cooper and Varela, 2015). However, they are too costly for deployment over large areas for extended periods of time. There are also concerns regarding the environmental sustainability of various bait technologies (Mercer et al., 2024). The development of biodegradable bait stations may offer a more environmentally appropriate delivery system, and one that would be suitable for organic producers (Le et al., 2024). In addition to the development of carrier- and species-appropriate bait formulations (e.g., sugar, protein, or sugar plus protein), further development and registration of effective active ingredients is needed. California also requires adjuvants be registered as pesticides. A greater emphasis on ant management in vineyards could provide a means to help suppress mealybug populations and increase the impact of other biological control strategies.
Little research has been conducted on the biocontrol of TCAH. Most natural enemies that have been identified are generalist arthropods and avian predators (Jordan, 1952); assassin and nabid bugs can also prey on less-mobile nymphal TCAH instars, but adults may escape predation because of their mobility and hard exoskeleton (UC IPM, n.d.). Nickerson et
___________________
8 See https://www.aphis.usda.gov/tradeimportsorganism-and-soil-imports/biological-control-organism-permits/microbial-organisms-used.
al. (1977) note that, similar to mealybugs, TCAH nymphs can be tended by ants, which may interfere with natural enemies attacking them. If TCAH is reproducing on non-crop plants within vineyards, ant management targeting mealybugs could have a benefit in TCAH management.
Conclusion 5-20: Parasitoids, predators, and EPFs have been identified that could be further studied for development as biocontrol agents for use in IPM programs targeting mealybugs.
Conclusion 5-21: EPF strains currently available for use on grapevines require repeated applications to be effective and may lose virulence when exposed to high temperatures and UV light; identification and mitigation of factors that degrade EPFs could help improve their utility in IPM programs or in situations where the use of chemical insecticides is not an option.
Conclusion 5-22: Because ants support mealybug survival in vineyards, more emphasis on ant management is needed to help suppress mealybug populations and increase the impact of other biocontrol strategies.
Conclusion 5-23: There is a dearth of research on biocontrol of TCAH; if research is pursued, it will be important to address the impacts of ants, which tend TCAH nymphs, on potential biocontrol agents.
Recommendation 5-9: Support research to find, evaluate, and develop more efficacious biocontrol agents and guide their integration with other management tactics within IPM programs or in situations, such as organic production systems, where chemical insecticides are not an option for vector management in grapevines.
SANITATION
Sanitation practices can help to prevent the spread of GLRaV-3 and GRBV by suppressing the spread of vector populations. Research is needed to identify the most effective and practical procedures to support sanitation and minimize the spread of vectors throughout a vineyard.
It is known that mealybug crawlers stick to workers’ clothing and vineyard tools and disperse among grapevines (Walton et al., 2009; Roda et al., 2013). The sanitation of workers’ protective covers, tools, and farming equipment was reported to be effective in limiting the dispersal of mealybugs in citrus orchards (Middleton and Diepenbrock, 2022). Spraying workers’ protective covers, small tools, and containers with commercially available isopropanol or hot water can be done to reduce the chances of
dispersing crawlers like mealybugs in vineyards. For farming equipment, the application of hot steam can kill most crawlers, although there is a need for further research to identify the optimum temperature and duration of steam applications to ensure efficacy (Hansen et al., 2011; Middleton and Diepenbrock, 2022).
In vineyards that employ mechanical strategies to harvest fruits or to thin and prune vines, insects can be disturbed by the equipment, causing them to spread more actively and accelerating dispersal of crawlers along the track of the moving machines (Charles et al., 2009). This can significantly increase the chances for dispersed viruliferous mealybugs to spread GLRaV-3. To reduce insect dispersal, mechanical equipment can be high-pressure washed with soapy water to remove plant stem, cane, and leaf debris that could carry crawlers; research is needed to determine the optimal frequency of washing to effectively reduce insect dispersal without negatively impacting vineyard operations and productivity. In addition, there may be opportunities to reduce the spread of vectors and virus by adjusting the order of operations in vineyards, such as by starting with blocks that are free of vectors or have lower densities before moving on to more extensively infested blocks. Dispersal across vine rows may be reduced by reorienting discharge chutes of machinery.
There is a general lack of information about best practices for sanitation in vineyard settings and the degree to which sanitation measures are employed is unknown. Research in other cropping systems indicates that the efficacy of cleaning programs varies with mealybug species and life stage (Middleton and Diepenbrock, 2022). In addition, since the biology and behavior of TCAH differ from those of mealybugs, sanitation of workers’ protective equipment, tools, and farming equipment may not be effective in reducing TCAH populations.
Conclusion 5-24: Cleaning harvesting and pruning equipment, tools, and workers’ protective equipment has been shown to limit the dispersal of mealybugs; however, there is a general lack of publicly available information about best practices for sanitation in vineyard settings, and the degree to which sanitation measures are employed is unknown.
Recommendation 5-10 (HP): Support research to determine the most effective and practical farm and worker equipment sanitation measures and harvesting and pruning strategies that can help minimize the spread of insect vectors.
PHYSICAL BARRIERS
Physical barriers can be used to prevent or discourage pests or disease vectors from accessing a crop. Three examples that may be relevant in the context of TCAH include fencing, kaolin clay, and reflective mulches.
Passive devices such as fencing can intercept pests as they fly toward a vineyard. The success and practicality of screening fences depend on the flight behavior of the target pest. Although data are limited, there may be opportunities use barrier screens to limit the movement of TCAH into vineyards from riparian areas. One study found that the vast majority of TCAH around soybean fields were captured near ground level (less than 33 centimeters above the surface) (Johnson and Mueller, 1989). Recent flight mill studies indicate that both male and female TCAH can travel hundreds of meters per day, but males fly substantially farther in individual flight sessions than do females (Antolínez et al., 2023).
In Florida, the tactic of installing protective screens over citrus trees has proven effective for growing trees in an enclosed environment and keeping them disease-free (Vashisth et al., 2021). However, this approach is expensive and likely to be most applicable for smaller acreages of specialty crops, such as fresh fruit varieties with a high return on investment. The use of individual protective covers (IPCs), protective mesh bags applied to individual trees, can be more economically feasible for varieties grown on large acreages (Gaire et al., 2022). IPCs provide an alternative to soil drenches and foliar insecticides, which cannot always prevent infection by the HLB pathogen (Candidatus Liberibacter asiaticus), especially in light of the increasing levels of psyllid resistance to neonicotinoid insecticides, which have been used extensively for almost a decade to protect young trees from the Asian citrus psyllid (Diaphorina citri). Psyllid exclusion by using IPCs is, therefore, a promising tool that has sparked interest in recent years, with many growers adopting this technology in citrus orchards in Florida (Alferez et al., 2021; Gaire et al., 2022, 2024).
The use of nets is considered a highly effective tactic for reducing bird damage to agricultural crops such as grapevines (Fuller-Perrine and Tobin, 1991; Taber and Martin, 1998). This tactic, which is becoming increasingly common in vineyards worldwide in response to changing bird migratory patterns, has been shown to have no detrimental effects on Cabernet franc yield or on the quality of the fruit and wine, especially when netting is installed early in the growing season (Pagay et al., 2013). The use of a net cover on grapevine, either on a vine row or individual vine, could be explored to exclude TCAH and other potential insect vectors of GRBV in vineyards in California. This tactic is more effective against flying insects; hence, it may not be effective against resident mealybugs within vineyards.
Whether it can limit the risk of vine infestation by immigrant (wind-aided) mealybug crawlers is unknown.
Kaolin clay applications leave a white, non-toxic residue on plant surfaces. This residue alters the physical appearance of plants and may also disrupt feeding by small insects, leading to reduced pathogen transmission (Reitz et al., 2008). Kaolin has been shown to interfere with the host plant settling and probing behavior of D. citri in citrus (Miranda et al., 2018); however, impacts on the behavior of TCAH have not been studied. Kaolin can also have diverse ancillary effects on the physiology of treated plants (Rosati, 2007); for grapes grown in Mediterranean climates, for example, kaolin applications mitigate physiological stresses from excess heat and drought conditions (Dinis et al., 2018). However, in a study conducted across multiple locations, kaolin treatments of vineyards in New Zealand and Italy were ineffective in controlling populations of Pseudococcus calceolariae, Ps. longispinus, and Pl. ficus (Tacoli et al., 2018).
Reflective mulches (i.e., aluminum or silver polyethylene mulches that reflect sunlight upward) can reduce the dispersal of insect pests into crops by disrupting the visual cues that insects need to locate potential host plants (Greer and Dole, 2003). In studies, the application of reflective mulches between crop rows reduced the abundance of leafhoppers in Cabernet franc grapes grown in Niagara, Canada (Coventry et al., 2005), Asian citrus psyllid in citrus (Croxton and Stansly, 2014), and vectors of Candidatus Phytoplasma pruni, the causal agent of X disease in cherry (Marshall et al., 2024). Marshall et al. (2024) noted that the reflective ground cover used in their study limits insect access to alternative host plants, which may further reduce vector populations within orchards. Coventry et al. (2005) also assessed effects on vine physiology and berry quality and found that the use of reflective mulches brought benefits for vine photosynthesis, advanced the timing of veraison, and increased levels of total soluble solids and total phenolics in berries. However, one downside is that these mulches deteriorate over time; Croxton and Stansly (2014) discuss potential opportunities to improve the longevity and durability of the materials.
Conclusion 5-25: Information about TCAH flight behavior and movement could be used to devise and evaluate possible physical barriers such as screening fences and kaolin clay to impede TCAH movement from riparian areas to vineyards.
Conclusion 5-26: Installing protective screens over citrus trees is effective for keeping them disease-free; however, this tactic is costly and may be most applicable for smaller acreages of crops with a high return on investment.
Conclusion 5-27: Covering individual vines with mesh bags may be a less costly tactic for vector exclusion; this approach has been widely adopted by citrus growers in Florida as an IPM tool to control HLB.
Conclusion 5-28: Reflective mulches have the potential to reduce leafhopper populations in grapes without any detrimental effects on vine physiology and berry quality; however, these mulches degrade over time.
Recommendation 5-11 (MP): Support research to evaluate the efficacy of physical barriers in deterring TCAH movement from natural or vineyard-adjacent habitats to vineyards.
Recommendation 5-12 (MP): Support research to evaluate the efficacy of reflective mulches in reducing the abundance of insect vectors in vineyards and research on improving the longevity and durability of reflective mulches.
AREAWIDE PEST MANAGEMENT
Areawide pest management (AWM), an approach for reducing pests by uniformly applying pest mitigation measures across large geographical areas instead of using a field-by-field approach, has the potential to facilitate management of both GLD and GRBD. This approach is particularly well suited for highly mobile pests or disease vectors (Hendrichs et al., 2007), and can overcome limitations farmers face when the activity of pests is on a larger spatial scale than that of the individual farms affected. For the bacterial disease HLB (citrus greening), citrus yields were positively correlated with the number of growers within a region participating in a coordinated AWM program (Singerman et al., 2017). However, despite the benefits, growers can be reluctant to participate in AWM programs, either from a preference to work independently or a lack of confidence that their neighbors will carry out the program mandates (Singerman et al., 2017), underscoring the need to build trust and educate stakeholders on the value of large-scale programs (Hendrichs et al., 2007).
In the context of GLD and GRBD, growers’ willingness to cooperate in AWM programs may be limited without outreach to ensure that they understand the severity of the disease threats and the long-term sustainability benefits of participating in areawide programs. Growers may be particularly hesitant to invest in programs in which they perceive that their investment disproportionately benefits neighboring competitors (Perring et al., 1999). The California grape industry has experience with AWM programs to support management of Pierce’s disease (Haviland et al., 2021), and lessons
from those programs can be used to develop and implement AWM programs for GLD and GRBD that attract broad participation among growers. Although they comprise a smaller scale than the California wine industry, production regions in New Zealand and South Africa have launched concerted, coordinated programs to manage GLD on an areawide basis (Pietersen et al., 2013; Chooi et al., 2024). Central to these programs are increased efforts to use virus-free material for planting, improved efforts to monitor and remove infected vines, and cooperative efforts to manage mealybug vectors across vineyards. These case studies can also provide valuable information for GLD and GRBD management in California.
Conclusion 5-29: Areawide pest management, which is well suited for pests that move beyond the boundaries of individual farms, can help in managing insect-vectored viruses in vineyards across larger areas.
Recommendation 5-13 (HP): Support efforts to develop areawide GLD and GRBD vector management programs for regions of California with different threat levels from these diseases, along with activities to encourage grower participation in these programs.
COORDINATING MANAGEMENT OF MULTIPLE VECTORS
Given the significance of Pierce’s disease as well as GLD and GRBD in California’s wine grape industry, it is imperative to coordinate management tactics for these different pathosystems to ensure that they are complementary, cost effective, and do not disrupt overall pest management. Since the vectors for all three diseases are hemipterans, insecticides that are effective against one species are likely to have activity against the other vectors. As a result, the timing of insecticide applications requires careful consideration to facilitate management of the entire vector complex, and it is important to be aware that applications can lead to insecticide resistance in species other than the one being targeted. In addition, if a pest is successfully managed through biological control, insecticide applications targeting other pests should minimize disruptions to biological control. Finally, the costs and benefits of tactics such as habitat manipulation should be weighed in the context of overall pest management.
Conclusion 5-30: Pierce’s disease, GLD, and GRBD are all spread by hemipterans, and insecticides used to control one vector species may also affect the other vectors; hence, it is important to coordinate vector management tactics for vectors of all three diseases.
HOST PLANT RESISTANCE TO VIRUSES AND VECTORS
Host plant resistance to plant viruses and insect vectors is an effective and sustainable approach for the control of vector-borne diseases. This approach relies on the plant defense response, which is driven by innate genetic traits in the plant. The availability of grapevine cultivars resistant to GLRaVs and GRBV (and/or their vectors) would have a long-term impact on the economics of wine grape production by increasing yields and quality, and could potentially reduce the inputs and costs associated with vector control. However, resistance traits must be carefully managed and would need to be part of a sustained IPM strategy for these vector-borne viruses.
Potential paths that can be explored for developing plants that are resistant to GLRaVs and GRBV include traditional breeding and bioengineering. Due to the complexity of the disease pathosystems, a multidisciplinary approach is essential, and any pathway would require the involvement of experts in plant breeding, plant biotechnology, plant virology, and vector biology. It is also important to screen for virus-resistant germplasm using the biological vectors (mealybugs and TCAH) to assess resistance (Djennane et al., 2021; Cousins, 2024), since the vector not only introduces biologically relevant amounts of the virus but may also deliver effector molecules that modulate plant defenses and create a favorable environment for virus replication (Ray and Casteel, 2022).
For traditional strategies using grape breeding and large-scale screens for genetic resistance, it is important to study both existing cultivars (Vitis vinifera) and wild grapes (other Vitis species), as resistance genes may be found in wild varieties or non-traditional varieties. This approach led to the successful identification of resistance genes for Pierce’s disease and grapevine fanleaf virus (Djennane et al., 2021; Huerta-Acosta et al., 2022). Using traditional breeding to screen for resistance genes and then incorporating them into commercially viable cultivars is time-consuming and labor-intensive, but can be rewarding. Identifying traits conferring resistance to Xylella fastidiosa, the causal agent of Pierce’s disease, was a research priority for over 20 years before the first wine grape cultivars incorporating the PdR1b resistance gene from V. arizonica were commercially released (Walker and Tenscher, 2019). Efforts to identify and incorporate additional X. fastidiosa resistance traits into V. vinifera cultivars are still in progress (Rapicavoli et al. 2018; Huerta-Acosta et al., 2022).
Once an effective resistance gene is identified, it can be transferred into popular wine cultivars using traditional breeding strategies or various bioengineering approaches. Bioengineering approaches such as RNA interference (RNAi)-based or transgenic resistance and genome editing can also be used to design and implement new genetic modifications that may yield effective, long-lasting resistance. Resistance to virtually any virus can
be created using knowledge of virus diversity and sequence conservation. RNAi-based resistance for plant viruses has been shown to be highly effective and durable for annual and perennial plants including plum (Scorza et al., 2013), papaya (Tripathi et al., 2007), squash (Tricoll et al., 1995), and bean (Aragão et al., 2013). Resistance to a geminivirus, bean golden mosaic virus, has been developed and deployed in beans for human consumption (Aragão et al., 2013). Such approaches could facilitate the development of a transgene that targets multiple genomic sequences in GLRaV-3 and GRBV. This would provide California wine grape growers with a single trait that provides protection from both virus threats, potentially with a lower regulatory burden than would be involved in obtaining approvals for multiple traits separately. Transgenic resistance mediated by RNAi may be one of the fastest and most effective approaches to get virus resistance into the field; several publications outlining best practices for RNAi-based plant virus resistance provide useful guidance in this endeavor (Zhao et al., 2019; Kumar et al., 2022), and the Pierce’s Disease/Glassy-Winged Sharpshooter Board has already supported research to develop RNAi-based resistance to GLRaV-3 and mealybug vectors.
Genome editing of susceptibility genes (genes that are required for the virus replication cycle in the plant) is another bioengineering pathway with increasing utility for non-model plants such as grapevines (Zhao et al., 2019; Khan et al., 2022). Filling the knowledge gaps of virus-host interactions may identify conserved host gene targets for directed mutation of downregulation or resistance genes for activation. It may be possible to target multiple GLRaVs and provide broad-spectrum resistance by modifying a conserved host factor. For example, there may be conserved pathways for GLRaV replication complex assembly that could be modified by genome editing with clustered regularly interspaced short palindromic repeats (CRISPR)/Cas to inhibit virus replication factory formation and confer resistance to viruses without compromising host growth under normal conditions. This approach would require detailed knowledge of the molecular virus-grapevine interactions that occur during virus infection. At this time, there is limited knowledge of such factors, although significant progress has been made toward genome editing in grapevines (Tricoli, 2024). A comprehensive analysis of GLRaV-3 and GRBV virus-host interactions in important wine grape cultivars and/or in the model grapevine cv. Pixie could facilitate further progress; the complex dynamics of GLD and GRBD in red or black- and white-fruited cultivars warrant fundamental studies employing contemporary tools in molecular biology, multi-omics, and plant biology to elucidate host-virus interactions using a systems biology approach to bridge the gap between genomics and phenomics of these diseases (Naidu et al., 2015). If susceptibility genes can be identified and modified with single-base changes, this may represent a path toward
disease resistance with minimal regulatory burden. Progress in genome editing approaches may also enable cisgenics (the modification of plants using a natural gene from a sexually compatible plant) to allow knock-in (i.e., insertion at a particular locus) incorporation of viral resistance genes identified using traditional breeding approaches into important wine grape cultivars.
In addition to conferring resistance to viral infections, similar bioengineering approaches can also be used to confer resistance to insect vectors. Researchers have made some progress toward identifying germplasm with resistance to mealybugs (Naegele et al., 2020). Genome editing of susceptibility genes in host plants is an additional avenue that could be explored for vector control.
At present, genome editing techniques are not subject to the same regulatory framework as genetically modified organisms in the United States because an edited genome also could potentially have been eventually produced through traditional breeding (Hundleby and Harwood 2022; Genetic Literacy Project, 2023). The lower regulatory standards could lead to faster commercialization of resistant cultivars developed through gene editing compared with RNAi-based transgenic approaches. However, detailed knowledge of virus-host interactions necessary for determining appropriate targets for edits has yet to be generated, and it is likely that separate gene targets for GLRaV-3 and GRBV will need to be identified.
For all host plant resistance approaches, a plan for moving the research from the lab to the field should be part of the research vision and is imperative for real-world application. These activities can include assessing potential off-target effects on grapevines and the quality of juice from new cultivars, full exploration of the regulatory hurdles required for approval, and consideration of consumer concerns and the acceptability of crops involving different types of bioengineering techniques.
Conclusion 5-31: Host plant resistance is an effective and sustainable tactic for controlling vector-borne virus diseases, especially when used as a component of an IPM strategy.
Conclusion 5-32: The choice of approach (traditional breeding or bioengineering strategies such as transgenic approaches or gene editing) for achieving host resistance has implications for the length of time required to create a resistant grapevine cultivar, the expediency of obtaining regulatory approval, and consumer acceptance.
Conclusion 5-33: RNAi-based resistance to plant viruses has been shown to be highly effective and durable for annual and perennial
crops; this approach could produce a resistant grape cultivar within a relatively short period of time.
Conclusion 5-34: Genome editing for developing host resistance to GLRaVs, GRBV, and their vectors requires knowledge of virus-host and vector-host interactions and the collaborative efforts of researchers from multiple disciplines.
Conclusion 5-35: Gene-edited crops are not subject to the same regulatory processes as genetically modified organisms in the United States and could therefore lead to faster commercialization of a resistant grapevine cultivar; however, information on virus-host and vector-host interactions necessary for determining appropriate edits is not yet available.
Recommendation 5-14 (HP): Support research using traditional and bioengineering approaches for developing GLD and GRBD resistance; when conducting resistance screening assays, the biological vector should be used as much as possible.
Recommendation 5-15: Support research on the use of transgenic RNAi for developing plants with virus and/or insect resistance; creating a transgene(s) combining resistance to GLRaV-3 and GRBV could provide effective resistance to both viruses and help reduce the burden of regulatory approval.
Recommendation 5-16: Develop grapevine as a model system to advance fundamental understanding of the entire network of virus-host interactions across cultivars.
Recommendation 5-17 (HP): Establish multidisciplinary and trans-institutional collaborations to enhance synergies in pursuing bioengineering approaches, such as RNAi-mediated resistance and CRISPR/Cas-based genome-editing technologies, as an alternative to traditional breeding for resistance against GLD and GRBD.
CROSS-PROTECTION STRATEGIES
Cross protection (also referred to as mild strain cross protection) is the use of a mild virus strain to infect a plant in order to protect it from subsequent infection by a more aggressive strain of the same virus that causes severe symptoms and damage. Cross protection has been applied to several important plant viruses, including in citrus against citrus tristeza virus
(CTV; Folimonova, 2013; Folimonova et al., 2020), in cacao against cacao swollen shoot virus (Ameyaw et al., 2016), in zucchini against zucchini yellow mosaic virus, and in tomato against pepino mosaic virus (Hernando and Aranda, 2024). One of the challenges in implementing cross protection is identifying suitable mild strains that induce protective effects across all phylogenetic groups of the same virus without causing damage to the plant or having a negative impact on crop yield, as occurred in efforts to develop cross protection for fanleaf degeneration (Komar et al., 2008; Vigne et al., 2009; Kubina et al., 2022).
Researchers have made some initial progress in laying the groundwork for developing cross-protection strategies for GLD. In 2013, Poojari et al. identified an asymptomatic strain of GLRaV-2 (designated as GLRaV-2-SG) that was found to have no significant effect on fruit yield, total soluble solids, juice pH, or total anthocyanins of berry skin in cv. Sangiovese. In 2019, Thompson et al. found a novel genetic variant of GLRaV-3 (designated as ID45) in Idaho and reported that the ID45 variant caused no foliar symptoms in Cabernet Sauvignon in the fall (Thompson et al., 2019); its effect on fruit yield or fruit quality has not been determined. However, the discovery of mild strains is only the first step in developing a cross-protection strategy for GLD management; the success of cross protection across grapevine cultivars under varying environmental conditions requires careful consideration of virus-host interactions and the impact of climate change events that can diminish grapevine responses to viral infections (Perrone et al., 2017; Velásquez et al., 2018). Moreover, despite efforts to understand the protection conferred using mild strains in initially infected plants, the molecular mechanism(s) behind cross protection remain(s) largely unclear (Zhang et al., 2018; Pechinger et al., 2019). Having a better understanding of the pathogenicity factors across all GLRaV-3 phylogenetic groups will be essential in developing a cross-protection strategy for GLD. Research into cross protection for GLD management could be guided by lessons learned from cross-protection efforts for other viruses, such as CTV (Folimonova, 2013), cacao swollen shoot virus (Ameyaw et al., 2016), sugarcane mosaic virus (Xu et al., 2021), and pepper mild mottle virus (Yoon et al., 2006).
Conclusion 5-36: The identification of a mild, asymptomatic strain of GLRaV-2 (GLRaV-2-SG) and a mild strain of GLRaV-3 (ID45) point to the potential to apply cross protection in GLD management.
Recommendation 5-18: Support research to explore cross protection as a possible tactic for managing GLD.
RISK ASSESSMENT MODELS TO GUIDE DECISION MAKING
GLRaV-3 and GRBV are two of the most economically damaging viruses that infect grapevines. Developing risk assessment models for GLRaV-3 and GRBV could enhance decision making and improve GLD and GRBD management. An example of such a model is the Bayesian Belief Network (BBN) model, which has been found to have application in forecasting crop diseases (Bi and Chen, 2011; Yang et al., 2019) and IPM decision making (Singh and Gupta, 2017). One advantage of the BBN model is that it provides a causally correct method to explore scenarios using both quantitative and qualitative inputs, distinguishing between statistical correlation and causal effects (Pearl, 2009, 2014; Topuz et al., 2023). It could be used to identify the risk factors associated with the highest likelihood of a GLRaV-3 or GRBV outbreak and to assess vineyard vulnerability to such a threat based on these identified risk factors. This model can also be used to inform the timing of insecticide applications to improve the effectiveness of GLRaV-3 and GRBV vector control. This type of model can provide a comprehensive framework for identifying the risk factors that increase the likelihood of a GLRaV-3 or GRBV outbreak and for assessing the relative risk of these factors either individually or in combination.
Conclusion 5-37: The Bayesian Belief Network model, which can be used to assess the probability of GLRaV-3 and GRBV outbreaks, could be helpful in informing GLD and GRBD management decision making.
Recommendation 5-19: Support research to evaluate the potential utility of the Bayesian Belief Network model in informing growers’ decisions related to GLRaV-3 and GRBV management.
RESEARCH PRIORITIZATION
High- and medium-priority research areas and actions (with the recommendation number) are summarized in Table 5-1 for quick reference. The recommended research and actions related to the use of clean plants, roguing, vector management, sanitation, physical barriers, and areawide pest management would contribute to GLD and GRBD management in the short term. Recommendations related to host plant resistance would contribute to GLD and GRBD management in the long term.
| High-Priority Research Areas and Actions |
|---|
| Encouraging the adoption and implementation of higher sanitary standards in registered mother blocks using robust, state-of-the-art, sensitive, and reliable diagnostic methods; roguing of infected vines to maintain disease-free stock (Recommendation 5-1) |
| Developing optimal roguing and replanting schemes and techniques to manage GLD and GRBD; facilitating their implementation by growers (Recommendation 5-2) |
| Determining the optimal conditions for application of systemic insecticides to achieve better mealybug control (Recommendation 5-3) |
| Developing and implementing insecticide resistance management programs and developing new active ingredients for mealybug management (Recommendation 5-4) |
| Determining the optimum conditions for the application of insecticides to achieve better TCAH control and to establish economic or action thresholds to guide insecticide application programs (Recommendation 5-5) |
| Generating information needed for improving efficacy of mating disruption for mealybug control; determining the benefits (economic and otherwise) of mating disruption as part of an integrated approach to manage insect vectors in grapevines (Recommendation 5-6) |
| Determining the most effective and practical farm and worker equipment sanitation measures and harvesting and pruning strategies that can help minimize spread of insect vectors (Recommendation 5-10) |
| Developing area-wide GLD and GRBD vector management programs for regions of California with different GLD and GRBD threat levels; activities to encourage grower participation in areawide programs (Recommendation 5-13) |
| Developing GLD and GRBD resistance using traditional and bioengineering approaches (Recommendation 5-14) |
| Establishing multidisciplinary and trans-institutional collaborations to enhance synergies in pursuing bioengineering approaches to develop GLD and GRBD resistance (Recommendation 5-17) |
| Medium-Priority Research Areas |
| Determining the costs and benefits of removing vegetation that harbors TCAH in and around vineyards and the use of trap crops to inform grower decision making (Recommendation 5-8) |
| Evaluating the efficacy of physical barriers in deterring TCAH movement from riparian areas to vineyards (Recommendation 5-11) |
| Evaluating the efficacy of reflective mulches in reducing the abundance of insect vectors in vineyards; improving the longevity and durability of reflective mulches (Recommendation 5-12) |
REFERENCES
Achala N. KC, J. B. DeShields, A. D. Levin, R. Hilton, and J. Rijal. 2022. Epidemiology of grapevine red blotch disease progression in Southern Oregon vineyards. American Journal of Enology and Viticulture 73:116-124.
Alferez, F., U. Albrecht, S. Gaire, O. Batuman, J. Qureshi, and M. Zekri. 2021. Individual protective covers (IPCs) for young tree protection from the HLB vector, the Asian citrus psyllid. HS1425, 10/2021. EDIS, 2021(5). https://edis.ifas.ufl.edu/publication/hs1425 (accessed August 14, 2024).
Almeida, R., K. Daane, V. Bell, G. K. Blaisdell, M. Cooper, E. Herrbach, and G. Pietersen. 2013. Ecology and management of grapevine leafroll disease. Frontiers in Microbiology 4:94.
Ameyaw, G. A., O. Domfeh, H. Dzahini-Obiatey, L. A. A. Ollennu, and G. K. Owusu. 2016. Appraisal of cocoa swollen shoot virus (CSSV) mild isolates for cross protection of cocoa against severe strains in Ghana. Plant Disease 100(4):810-815. https://doi.org/10.1094/PDIS-09-15-0974-RE_(accessed July 31, 2024).
Antolínez, C. A., M. Chandler, V. Hoyle, M. Fuchs, and M. J. Rivera. 2023. Differential flight capacity of Spissistilus festinus (Hemiptera: Membracidae) by sex and age. Journal of Insect Behavior 36:347-357.
Aragão, F. J., E. O. Nogueira, M. L. P. Tinoco, and J. C. Faria. 2013. Molecular characterization of the first commercial transgenic common bean immune to the bean golden mosaic virus. Journal of Biotechnology 166(1-2):42-50.
Bahder, B. W., R. A. Naidu, K. M. Daane, J. G. Millar, and D. B. Walsh. 2013. Pheromone-based monitoring of Pseudococcus maritimus (Hemiptera: Pseudococcidae) populations in concord grape vineyards. Journal of Economic Entomology 106(1):482-490.
Bell, V. A., R. G. E. Bonfiglioli, J. T. S. Walker, P. L. Lo, J. F. Mackay, and S. E. McGregor. 2009. grapevine leafroll-associated virus 3 persistence in Vitis vinifera remnant roots. Journal of Plant Pathology 91:527-533.
Bell, V. A., P. J. Lester, G. Pietersen, and A. J. Hall. 2021. The management and financial implications of variable responses to grapevine leafroll disease. Journal of Plant Pathology 103:5-15.
Benelli, G., A. Lucchi, D. Thomson, and C. Ioriatti. 2019. Sex pheromone aerosol devices for mating disruption: Challenges for a brighter future. Insects 10(10):308.
Beyer, B. A., R. Srinivasan, P. M. Roberts, and M. R. Abney. 2017. Biology and management of the three-cornered alfalfa hopper (Hemiptera: Membracidae) in alfalfa, soybean, and peanut. Journal of Integrated Pest Management 8(1):10.
Bi, C., and G. Chen. 2011. Bayesian networks modeling for crop diseases. In Computer and Computing Technologies in Agriculture IV: 4th IFIP TC 12 Conference, CCTA 2010, Nanchang, China, October 22-25, 2010, Selected Papers, Part I 4. Springer Berlin Heidelberg. Pp. 312-320.
Bick, E. N., C. R. Kron, and F. G. Zalom. 2020. Timing the implementation of cultural practices for Spissistilus festinus (Hemiptera: Membracidae) in California vineyards using a stage-structured degree-day model. Journal of Economic Entomology 113:2558-2562.
Billings, A. C., K. Flores, K. A. McCalla, K. M. Daane, and H. Wilson. 2021. Use of ground covers to control three-cornered alfalfa hopper, Spissistilus festinus (Hemiptera: Membracidae), and other suspected vectors of Grapevine red blotch virus. Journal of Economic Entomology 114:1462-1469.
Bradley, S., and T. Kuhar. 2023. Survey of insecticide efficacy on three-cornered alfalfa hopper. Virginia Cooperative Extension ENTO-555NP. https://www.pubs.ext.vt.edu/content/dam/pubs_ext_vt_edu/ENTO/ento-555/ENTO-555.pdf (accessed July 22, 2024).
Cardwell, K., G. Dennis, A. R. Flannery, J. Fletcher, D. Luster, M. Nakhla, A. Rice, P. Shiel, J. Stack, C. Walsh, and L. Levy. 2018. Principles of diagnostic assay validation for plant pathogens: A basic review of concepts. Plant Health Progress 19:272-278.
CDPR (California Department of Pesticide Regulation). 2023. Accelerating Sustainable Pest Management: A Roadmap for California. https://www.cdpr.ca.gov/docs/sustainable_pest_management_roadmap/spm_roadmap.pdf (accessed August 29, 2024).
Charles, J. G., K. J. Froud, R. van den Brink, and D. J. Allan. 2009. Mealybugs and the spread of grapevine leafroll-associated virus 3 (GLRaV-3) in a New Zealand vineyard. Australasian Plant Pathology 38:576-583
Chooi, K. M., D. Cohen, and M. N. Pearson. 2013. Generic and sequence-variant specific molecular assays for the detection of the highly variable grapevine leafroll-associated virus 3. Journal of Virological Methods 189:20-29.
Chooi, K. M., V. A. Bell, A. G. Blouin, M. Sandanayaka, R. Gough, A. Chhagan, and R. M. MacDiarmid. 2024. The New Zealand perspective of an ecosystem biology response to grapevine leafroll disease. Advances in Virus Research 118:213-272.
Cieniewicz, E., M. Flasco, M. Brunelli, A. Onwumelu, A. Wise, and M. F. Fuchs. 2019. Differential spread of grapevine red blotch virus in California and New York vineyards. Phytobiomes Journal 3:203-211.
Cocco, A., A. Lentini, and G. Serra. 2014. Mating disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in vineyards using reservoir pheromone dispensers. Journal of Insect Science 14:144. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5443473/ (accessed July 31, 2024).
Cocco, A., E. Muscas, A. Mura, A. Iodice, F. Savino, and A. Lentini. 2018. Influence of mating disruption on the reproductive biology of the vine mealybug, Planococcus ficus (Hemiptera: Pseudococcidae), under field conditions. Pest Management Science 74(12):2806-2816.
Cooper, M. L., and L. G. Varela. 2015. Evaluation of commercial ant baits as a component of an integrated pest management program for vine mealybug. Renewal Progress Report for CDFA Agreement number 15-0219-SA. https://static.cdfa.ca.gov/PiercesDisease/reports/2016/Progress%20Rpt_Cooper_Varela_Argentine%20ant%20bait%20for%20VMB_final.pdf (accessed on July 29.2024).
Cousins, P. 2024. Grape breeding. Presentation at the National Academies of Sciences, Engineering, and Medicine Open Session, March 4, 2024.
Coventry, J. M., K. H. Fisher, J. N. Strommer, and A. G. Reynolds. 2005. Reflective mulch to enhance berry quality in Ontario wine grapes. Acta Horticulturae 689:95-102.
Croxton, S. D., and P. A. Stansly. 2014. Metalized polyethylene mulch to repel Asian citrus psyllid, slow spread of Huanglongbing and improve growth of new citrus plantings. Pest Management Science 70:318-323.
Cunniffe, N. J., N. P. Taylor, F. M. Hamelin, and M. J. Jeger. 2022. Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission. PLOS Computational Biology 17:e1009759.
Daane, K. M., K. R. Sime, J. Fallon, and M. L. Cooper. 2007. Impacts of Argentine ants on mealybugs and their natural enemies in California’s coastal vineyards. Ecological Entomology 32:583-596.
Daane, K. M., M. L. Cooper, K. R. Sime, E. H. Nelson, M. C. Battany, and M. K. Rust. 2008. Testing baits to control Argentine ants (Hymenoptera: Formicidae) in vineyards. Journal of Economic Entomology 101:699-709.
Daane, K. M., R. P. P. Almeida, V. A. Bell, J. T. S. Walker, M. Botton, M. Fallahzadeh, M. Mani, J. L. Miano, R. Sforza, V. M. Walton, and T. Zaviezo. 2012. Chapter 12: Biology and management of mealybugs in vineyards. In Arthropod management in vineyards: Pests, approaches and future directions, edited by N. J. Bostanian, C. Vincent, and R. Isaacs. Netherlands: Springer. Pp. 271-307.
Daane, K., W. J. Bentley, R. J. Smith, D. R. Haviland, E. A. Weber, M. C. Battany, C. A. Gisbert, and J. G. Millar. 2013. Planococcus mealybugs (Vine mealybug). In Grape Pest Management, Vol. 3343, edited by L. J. Bettega. UCANR Publications. Pp. 246.
Daane, K. M., G. Y. Yokota, V. M. Walton, B, N. Hogg, M. L. Cooper, W. J. Bentley, and J. G. Millar. 2020. Development of a mating disruption program for a mealybug, Planococcus ficus, in vineyards. Insects 11(9):635.
Daane, K. M., M. L. Cooper, N. H. Mercer, B. N. Hogg, G. Y. Yokota, D. R. Haviland, S. C. Welter, F. E. Cave, A. A. Sial, and E. A. Boyd. 2021. Pheromone deployment strategies for mating disruption of a vineyard mealybug. Journal of Economic Entomology 114(6):2439-2451.
Daane, K., and D. Haviland. 2024. Sustainable Control Tools for Vine Mealybug. Wine Business Monthly May 2024, https://www.winebusiness.com/wbm/article/286237 (accessed July 25, 2024).
Deza-Borau, G., M. L. Peschiutta, V. D. Brito, V. L. Usseglio, M. P. Zunino, and J. A. Zygadlo. 2020. Development of novel bioinsecticides for organic control of Planococcus ficus in vineyards. Vitis 59:127-132. https://core.ac.uk/download/pdf/328003362.pdf (accessed November 14, 2024).
Diaz-Lara, A., V. Klaassen, K. Stevens, M. R. Sudarshana, A. Rowhani, H. J. Maree, K. M. Chooi, A. G. Blouin, N. Habili, Y. Song, K. Aram, K. Arnold, M. L. Cooper, L. Wunderlich, M. C. Battany, L. R. Bettiga, R. J. Smith, R. Bester, H. Xiao, B. Meng, J. E. Preece, D. Golino, and M. Al Rwahnih. 2018. Characterization of grapevine leafroll-associated virus 3 genetic variants and application towards RT-qPCR assay design. PLoS ONE 13(12):e0208862. Published online 2018 Dec 12. https://doi.org/10.1371/journal.pone.0208862 (accessed August 29, 2024).
Dinis, L. T., S. Bernardo, A. Luzio, G. Pinto, M. Meijón, M. Pintó-Marijuan, A. Cotado, C. Correia, and J. Moutinho-Pereira. 2018. Kaolin modulates ABA and IAA dynamics and physiology of grapevine under Mediterranean summer stress. Journal of Plant Physiology 220:181-192.
Djennane, S., E. Prado, V. Dumas, G. Demangeat, S. Gersch, A. Alais, C. Gertz, M. Beuve, O. Lemaire, and D. Merdinoglu. 2021. A single resistance factor to solve vineyard degeneration due to grapevine fanleaf virus. Communications Biology 4(1):637.
Dumont, F., and C. Provost. 2022. Using autumnal trap crops to manage tarnished plant bugs (Lygus lineolaris). Insects 13:441.
Dupuis, B., J. Cadby, G. Goy, M. Tallant, J. Derron, R. Schwaerzel, and T. Steinger. 2017. Control of potato virus Y (PVY) in seed potatoes by oil spraying, straw mulching and intercropping. Plant Pathology 66(6):960-969.
Duso, C., A. Pozzebon, M. Lorenzon, D. Fornasiero, P. Tirello, S. Simoni, and B. Bagnoli. 2022. The impact of microbial and botanical insecticides on grape berry moths and their effects on secondary pests and beneficials. Agronomy 12(1):217.
Farrar, J. J., M. E. Baur, and S. F. Elliott. 2016. Adoption of IPM practices in grape, tree fruit, and nut production in the Western United States. Journal of Integrated Pest Management 7(1). https://doi.org/10.1093/jipm/pmw007 (accessed July 30, 2024).
Figadère, B. A., J. S. McElfresh, D. Borchardt, K. M. Daane, W. Bentley, and J. G. Millar. 2007. Trans-α-necrodyl isobutyrate, the sex pheromone of the grape mealybug, Pseudococcus maritimus. Tetrahedron Letters 48:8434-8437.
Folimonova, S. Y. 2013. Developing an understanding of cross-protection by citrus tristeza virus. Frontiers in Microbiology 4:76. https://doi.org/10.3389/fmicb.2013.00076/full (accessed July 30, 2024).
Folimonova, S.Y., D. Achor, and M. Bar-Joseph. 2020. Walking together: Cross-protection, genome conservation, and the replication machinery of citrus tristeza virus. Viruses 12(12):1353, https://doi.org/10.3390/v12121353 (accessed September 3, 2024).
Fuller-Perrine, L. D., and M. E. Tobin. 1991. A cost-effective method for applying and removing bird-exclusion netting in commercial vineyards. https://digitalcommons.usu.edu/wdmconference/1991/all1991/18/ (accessed August 18, 2024).
Fuxa, J. 1987. Ecological considerations for the use of entomopathogens in IPM. Annual Review of Entomology 32:225-251.
Gaire, S., U. Albrecht, O. Batuman, J. Qureshi, M. Zekri, and F. Alferez. 2022. Individual protective covers (IPCs) to prevent Asian citrus psyllid and Candidatus Liberibacter asiaticus from establishing in newly planted citrus trees. Crop Protection 152. https://doi.org/10.1016/j.cropro.2021.105862 (accessed August 5, 2024).
Gaire, S., U. Albrecht, O. Batuman, M. Zekri, and F. Alferez. 2024. Individual protective covers improve yield and quality of citrus fruit under endemic Huanglongbing. Plants 13(16):2284. https://doi.org/10.3390/plants13162284 (accessed September 3, 2024).
Garzo, E., A. Moreno, M. Plaza, and A. Fereres. 2020. Feeding behavior and virus-transmission ability of insect vectors exposed to systemic insecticides. Plants 9:895.
Genetic Literacy Project. 2023. Overview of CRISPR and Gene Editing. Gene-edited crops are regulated as conventional plants with minimal restrictions and no necessary safety assessment. https://crispr-gene-editing-regs-tracker.geneticliteracyproject.org/united-states-cropsfood/ (accessed July 22, 2024).
Grasswitz, T. R., and D. G. James. 2008. Movement of grape mealybug, Pseudococcus maritimus, on and between host plants. Entomologia Experimentalis et Applicata 129:268-275.
Greer, L., and J. M. Dole. 2003. Aluminum foil, aluminum-painted, plastic, and degradable mulches increase yields and decrease insect-vectored viral diseases in vegetables. Hort Technology 13:276-284.
Gutierrez, A. P., K. M. Daane, L. Ponti, V. M. Walton, and C. K. Ellis. 2008. Prospective evaluation of the biological control of vine mealybug: Refuge effects and climate. Journal of Applied Ecology 45:524-536.
Hamby, K. A., N. L. Nicola, F. J. A. Niederholzer, and F. G. Zalom. 2015. Timing spring insecticide applications to target both Amyelois transitella (Lepidoptera: Pyralidae) and Anarsia lineatella (Lepidoptera: Gelechiidae) in almond orchards. Journal of Economic Entomology 108:683-693.
Hamim, I., J. Y. Suzuki, W. B. Borth, M. J. Melzer, M. M. Wall, and J. S. Hu. 2022. Preserving plant samples from remote locations for detection of RNA and DNA viruses. Frontiers in Microbiology 13:930329. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9453036/ (accessed August 29, 2024).
Hansen, J. D., J. A. Johnson, and D. A. Winter. 2011. History and use of heat in pest control: A review. International Journal of Pest Management 57:267-289
Haviland, D. R., B. Stone-Smith, and M. Gonzalez. 2021. Control of Pierce’s disease through areawide management of glassy-winged sharpshooter (Hemiptera: Cicadellidae) and roguing of infected grapevines. Journal of Integrated Pest Management 12(1). https://doi.org/10.1093/jipm/pmab008 (accessed July 30, 2024).
Hendrichs, J., P. Kenmore, A. Robinson, and M. J. B. Vreysen. 2007. Area-wide integrated pest management (AW-IPM): Principles, practice and prospects. In Area-wide control of insect pests from research to field implementation, edited by M. J. B. Vreysen, A. S. Robinson, and J. Hendrichs. Dordrecht, The Netherlands: Springer. Pp. 3-33.
Hernando, Y., and M. A. Aranda. 2024. Cross-protection against pepino mosaic virus, more than a decade of efficient disease control. Annals of Applied Biology 184(2):174-182. https://onlinelibrary.wiley.com/action/showCitFormats?doi=10.1111%2Faab.12884 (accessed July 30, 2024).
Hobbs, M. B., S. M. Vengco, S. L. Bolton, L. J. Bettiga, M. M. Moyer, and M. L. Cooper. 2022. Adoption of best management practices for grapevine leafroll and red blotch diseases: A survey of west coast growers. PhytoFrontiers 2:181-191.
Hogg, B. N., M. L. Cooper, and K. M. Daane. 2021. Areawide mating disruption for vine mealybug in California vineyards. Crop Protection 148:105735.
Huerta-Acosta, K. G., S. Riaz, A. Tenscher, and M. A. Walker. 2022. Genetic characterization of Pierce’s disease resistance in a Vitis arizonica/monticola wild grapevine. American Journal of Enology and Viticulture 2022: jev.2022.22021. https://doi.org/10.5344/ajev.2022.22021.
Hundleby, P., and W. Harwood. 2022. Regulatory constraints and differences of genome-edited crops around the globe. In Genome editing: Current technology advances and applications for crop improvement, edited by S. H. Wani and G. Hensel. Cham: Springer International Publishing. Pp. 319-341, https://doi.org/10.1007/978-3-031-08072-2_17 (accessed July 30, 2024).
Hunt, R. E. 1993. Role of vibrational signals in mating behavior of Spissistilus festinus (Homoptera: Membracidae). Annals of the Entomological Society of America 86:356-361.
Jaronski, S. T. 2010. Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55:159-185.
Javaran, V. J., A. Poursalavati, P. Lemoyne, D. T. Ste-Croix, P. Moffett, and M. L. Fall. 2023. NanoViromics: Long-read sequencing of dsRNA for plant virus and viroid rapid detection. Frontiers in Microbiology 14:1192781. https://doi.org/10.3389/fmicb.2023.1192781 (accessed August 29, 2024).
Johnson, M. P., and A. J. Mueller. 1989. Flight activity of the three-cornered alfalfa hopper (Homoptera: Membracidae) in soybean. Journal of Economic Entomology 82:1101-1105.
Johnson, M. P., and A. J. Mueller. 1990. Flight and diel activity of the three-cornered alfalfa hopper (Homoptera: Membracidae). Environmental Entomology 19(3):677-683. https://doi.org/10.1093/ee/19.3.677.
Jordan Jr., C. R. 1952. The biology and control of the three-cornered alfalfa hopper Spissistilus festinus (Say). PhD. diss., Jordan Jr., Cedric Roy: Texas A&M University, College Station, TX.
Khan, Z. A., R. Kumar, and I. Dasgupta. 2022. CRISPR/Cas-mediated resistance against viruses in plants. International Journal of Molecular Sciences 23(4):2303. https://www.mdpi.com/1422-0067/23/4/2303 (accessed July 30, 2024).
Komar, V., E. Vigne, G. Demangeat, O. Lemaire, and M. Fuchs. 2008. Cross-protection as control strategy against grapevine fanleaf virus in naturally infected vineyards. Plant Disease 92(12):1689-1694.
Kron, C. R., and M. S. Sisterson. 2020. Identification of nonhost cover crops of the three-cornered alfalfa hopper (Spissistilus festinus). American Journal of Enology and Viticulture 71(3):175-180.
Kubina, J., J. M. Hily, P. Mustin, V. Komar, S. Garcia, I. R. Martin, N. Poulicard, A. Velt, V. Bonnet, L. Mercier, O. Lemaire, and E. Vigne. 2022. Characterization of grapevine fanleaf virus isolates in ‘Chardonnay’ vines exhibiting severe and mild symptoms in two vineyards. Viruses 14(10):2303, https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9609649/ (accessed July 30, 2024).
Kumar, K. K., S. Varanavasiappan, L. Arul, E. Kokiladevi, and D. Sudhakar. 2022. Strategies for efficient RNAi-based gene silencing of viral genes for disease resistance in plants. In Plant gene silencing methods in molecular biology, Vol 2408, edited by K. S. Mysore and M. Senthil-Kumar. New York, NY: Humana. Pp. 23-35. https://doi.org/10.1007/978-1-0716-1875-2_2 (accessed July 30, 2024).
Kurwadkar, S. T., D. Dewinne, R. Wheat, D. G. McGahan, and F. L. Mitchell. 2013. Time dependent sorption behavior of dinotefuran, imidacloprid and thiamethoxam. Journal of Environmental Science and Health Part B 48:237-242.
Le, B., K. Campbell, H. Park, S.-P. Tseng, R. Pandey, G. S. Simmons, R. Henderson, C. Gispert, M. K. Rust, and C.-Y. Lee. 2024. Field evaluations of biodegradable boric acid hydrogel baits for the control of Argentine ants: Promising results in vineyards and citrus orchards. California Agriculture 78.
Levi-Zada, A., D. Fefer, M. David, M. Eliyahu, J. C. Franco, A. Protasov, E. Dunkelblum, and Z. Mendel. 2014. Diel periodicity of pheromone release by females of Planococcus citri and Planococcus ficus and the temporal flight activity of their conspecific males. Naturwissenschaften 101:671-678.
Li, J., J. Troendle, M. I. Gómez, J. Ifft, D. Golino, and M. Fuchs. 2022. Returns to public investments in clean plant centers: A case study of leafroll virus-tested grapevines in support of cost-effective grape production systems. Journal of Wine Economics 17:209-224.
Lima, P. J. 1992. USDA pest risk assessment of biological control organisms. EPPO Bulletin 22:475-478. https://doi.org/10.1111/j.1365-2338.1992.tb00531.x (accessed July 30, 2024).
Lucchi, A., and G. Benelli. 2018. Towards pesticide-free farming? Sharing needs and knowledge promotes integrated pest management. Environmental Science and Pollution Research 25:13439-13445.
Lucchi, A., P. Suma, E. Ladurner, A. Iodice, F. Savino, R. Ricciardi, F. Cosci, E. Marchesini, G. Conte, and G. Benelli. 2019. Managing the vine mealybug, Planococcus ficus, through pheromone-mediated mating disruption. Environmental Science and Pollution Research 26:10708-10718.
Malakar-Kuenen, R., K. M. Daane, W. Bentley, G. Yokota, L. Martin, K. Godfrey, and J. Ball. 2001. Population dynamics of the vine mealybug and its natural enemies in the Coachella and San Joaquin Valleys. University of California Plant Protection Quarterly 11:1-3.
Mankin, R. 2012. Applications of acoustics in insect pest management. CABI Reviews:1-7, https://www.cabidigitallibrary.org/doi/10.1079/PAVSNNR20127001(accessed July 30, 2024).
Mannini, F., and M. Digiaro. 2017. The Effects of viruses and viral diseases on grapes and wine. In Grapevine viruses: Molecular biology, diagnostics and management, edited by B. Meng, G. P. Martelli, D. A. Golino and M. Fuchs. Cham: Springer International Publishing. Pp. 453-482, https://doi.org/10.1007/978-3-319-57706-7_23 (accessed July 30, 2024).
Mansour, R., K. Grissa-Lebdi, M. Khemakhem, I. Chaari, I. Trabelsi, A. Sabri, and S. Marti. 2017. Pheromone-mediated mating disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in Tunisian vineyards: Effect on insect population dynamics. Biologia 72(3):333-341.
Maree, H. J., M. D. Pirie, K. Oosthuizen, R. Bester, D. J. G. Rees, and J. T. Burger. 2015. Phylogenomic analysis reveals deep divergence and recombination in an economically important grapevine virus. PLoS ONE 10:e0126819.
Marshall, A. T., T. D. Melton, G. Bishop, A. E. Clarke, C. A. Reyes-Corral, K. A. Catron, L. B. Nottingham, and T. D. Northfield. 2024. Cultural control methods improve management of leafhopper vector of X-disease. Crop Protection 175:106445.
Martin, T. R. 2021. Improving vine mealybug Planococcus ficus controls through adjuvant addition in major grape growing regions of California. Master’s thesis, Martin, T. R.: California State University, Fresno.
Massart, S., I. Adams, M. Al Rwahnih, S. Baeyen, G. J. Bilodeau, A. G. Blouin, and B. S. Lebas. 2022. Guidelines for the reliable use of high throughput sequencing technologies to detect plant pathogens and pests. Peer Community Journal 2:e62.
McDaniel, A. L., M. Mireles, D. Gadoury, T. Collins, and M. M. Moyer. 2024a. Effects of ultraviolet-C light on grapevine powdery mildew and fruit quality in Vitis vinifera Chardonnay. American Journal of Enology and Viticulture 75: 0750014.
McDaniel, A. L., D. M. Gadoury, and M. M. Moyer. 2024b. Effects of germicidal ultraviolet-C light on grape mealybug (Pseudococcus maritimus). Crop Protection 178:106584.
McGhee, P. S. 2014. Impact of high releasing mating disruption formulations on (male) codling moth, Cydia pomonella L., behavior. PhD diss., McGhee, Peter Scott: Michigan State University, East Lansing, MI. Pp. 133. https://d.lib.msu.edu/etd/3126 (accessed July 31, 2024).
Mercer, N., D. Haviland, and K. Daane. 2024 (unpublished). Mealybug, Planococcus Ficus, suppression through pavement ant, Tetramorium Immigrans, management using polyacrylamide hydrogel baits in vineyards. Unpublished preprint. https://papers.ssrn.com/sol3/papers.cfm?abstract_id=4924755 (accessed October 23, 2024).
Mermer, S., F. Pfab, G. Tait, R. Isaacs, P. D. Fanning, S. Van Timmeren, G. M. Loeb, S. P. Hesler, A. A. Sial, J. H. Hunter, H. K. Bal, F. Drummond, E. Ballman, J. Collins, L. Xue, D. Jiang, and V. M. Walton. 2021. Timing and order of different insecticide classes drive control of Drosophila suzukii: A modeling approach. Journal of Pest Science 94:743-755.
Middleton, E. G., and L. M. Diepenbrock. 2022. Sanitizing equipment and personnel to prevent the spread of hibiscus mealybug Nipaecoccus viridis (Hemiptera: Pseudococcidae) in Florida citrus. Journal of Economic Entomology 115:1592-1600.
Millar, J. G., K. M. Daane, J. S. Mcelfresh, J. A. Moreira, R. Malakar-Kuenen, M. Guillén, and W. J. Bentley. 2002. Development and optimization of methods for using sex pheromone for monitoring the mealybug Planococcus ficus (Homoptera: Pseudococcidae) in California vineyards. Journal of Economic Entomology 95:706-714.
Millar, J. G., S. L. Midland, J. S. McElfresh, and K. M. Daane. 2005. (2,3,4,4-tetramethyl-cyclopentyl)methyl acetate, a sex pheromone from the obscure mealybug: First example of a new structural class of monoterpenes. Journal of Chemical Ecology 31:2999-3005.
Millar, J. G., J. A. Moreira, J. S. McElfresh, K. M. Daane, and A. S. Freund. 2009. Sex pheromone of the longtailed mealybug: A new class of monoterpene structure. Organic Letters 11:2683-2685.
Miller, J. R., and L. J. Gut. 2015. Mating disruption for the 21st century: Matching technology with mechanism. Environmental Entomology 44(3):427-453.
Miller, J. R., L. J. Gut, F. M. De Lame, and L. L. Stelinski. 2006. Differentiation of competitive vs. non-competitive mechanisms mediating disruption of moth sexual communication by point sources of sex pheromone (Part I): Theory. Journal of Chemical Ecology 32:2089-2114.
Miranda, M. P., O. Z. Zanardi, A. F. Tomaseto, H. X. Volpe, R. B. Garcia, and E. Prado. 2018. Processed kaolin affects the probing and settling behavior of Diaphorina citri (Hemiptera: Lividae). Pest Management Science 74:1964-1972.
Mitchell, P. L., and L. D. Newsom. 1984. Seasonal history of the three-cornered alfalfa hopper (Homoptera: Membracidae) in Louisiana. Journal of Economic Entomology 77:906-914.
Montemayor, J. D., H. A. Smith, N. A. Peres, and S. Lahiri. 2023. Potential of UV-C for management of two-spotted spider mites and thrips in Florida strawberry. Pest Management Science 79(2):891-898.
Naegele, R. P., P. Cousins, and K. M. Daane. 2020. Identification of Vitis cultivars, rootstocks, and species expressing resistance to a Planococcus mealybug. Insects 11(2):86.
Naidu, R. A., H. J. Maree, and J. T. Burger. 2015. Grapevine leafroll disease and associated viruses: A unique pathosystem. Annual Review of Phytopathology 53:613-634.
Nickerson, J., C. R. Kay, L. Buschman, and W. Whitcomb. 1977. The presence of Spissistilus festinus as a factor affecting egg predation by ants in soybeans. The Florida Entomologist 60(3):193-199.
O’Hearn, J. S., and D. B. Walsh. 2020. Effectiveness of imidacloprid, spirotetramat, and flupyradifurone to prevent spread of GLRaV-3 by grape mealybug, Pseudococcus maritimus (Hemiptera: Pseudococcidae). Journal of Plant Diseases and Protection 127:805-809.
Onofre, R. B., D. M. Gadoury, A. Stensvand, A. Bierman, M. Rea, and N. A. Peres. 2021. Use of ultraviolet light to suppress powdery mildew in strawberry fruit production fields. Plant Disease 105(9):2402-2409.
Ovalle, C., A. del Pozo, M. B. Peoples, and A. Lavín. 2010. Estimating the contribution of nitrogen from legume cover crops to the nitrogen nutrition of grapevines using a 15N dilution technique. Plant and Soil 334:247-259.
Pagay, V., A. G. Reynolds, and K. H. Fisher. 2013. The influence of bird netting on yield and fruit, juice, and wine composition of Vitis vinifera L. Journal International Des Sciences De La Vigne Et Du Vin 47:35-45.
Pearl, J. 2009. Causal inference in statistics: An overview. Statistics Surveys 3:96-146.
Pearl, J. 2014. Probabilistic reasoning in intelligent systems: Networks of plausible inference. Elsevier. 552 pp.
Pechinger, K., K. M. Chooi, R. M. MacDiarmid, S. J. Harper, and H. Ziebell, H. 2019. A new era for mild strain cross-protection. Viruses 11:670.
Perring, T. M., N. M. Gruenhagen, and C. A. Farrar. 1999. Management of plant viral diseases through chemical control of insect vectors. Annual Review of Entomology 44:457-481.
Perrone, I., W. Chitarra, P. Boccacci, and G. Gambino. 2017. Grapevine–virus–environment interactions: An intriguing puzzle to solve. New Phytologist 213:983-987.
Pietersen, G., N. Spreeth, T. Oosthuizen, A. van Rensburg, M. van Rensburg, D. Lottering, N. Rossouw, and D. Tooth. 2013. Control of grapevine leafroll disease spread at a commercial wine estate in South Africa: A case study. American Journal of Enology and Viticulture 64:296-305.
Pietersen, G. 2024. Grapevine leafroll disease (GLD) and its management in South Africa. Presentation at the National Academies of Sciences, Engineering, and Medicine Open Session, May 2024.
PM 7/151(1). 2022. Considerations for the use of high throughput sequencing in plant health diagnostics. EPPO Bulletin 52:619-642, https://doi.org/10.1111/epp.12884 (accessed August 29, 2024).
Polajnar, J., A. Eriksson, M. Virant-Doberlet, A. Lucchi, and V. Mazzoni. 2016. Developing a bioacoustic method for mating disruption of a leafhopper pest in grapevine. In Advances in insect control and resistance management, edited by A. R. Horowitz and I. Ishaaya. Cham: Springer International Publishing. Pp. 165-190.
Poliakon, R. A., R. A. van Steenwyk, A. M. Hernandez, B. J. Wong, and P. S. Verdegaal. 2017. Control of vine mealybug, Planococcus ficus, in wine grapes using new reduced-risk insecticides in a pest management program. IOBC/WPRS Bulletin 128:102-109.
Poojari, S., O. J. Alabi, and R. A. Naidu. 2013. Molecular characterization and impacts of a strain of grapevine leafroll-associated virus 2 causing asymptomatic infection in a wine grape cultivar. Virology Journal 10:1-5.
Prabhaker, N., S. Castle, F. Byrne, T. J. Henneberry, and N. C. Toscano. 2006. Establishment of baseline susceptibility data to various insecticides for Homalodisca coagulata (Homoptera: Cicadellidae) by comparative bioassay techniques. Journal of Economic Entomology 99:141-154.
Preto, C. R., B. W. Bahder, E. N. Bick, M. R. Sudarshana, and F. G. Zalom. 2019. Seasonal dynamics of Spissistilus festinus (Hemiptera: Membracidae) in a Californian vineyard. Journal of Economic Entomology 112:1138-1144
Rapicavoli, J., B. Ingel, B. Blanco-Ulate, D. Cantu, and C. Roper. 2018. Xylella fastidiosa: An examination of a re-emerging plant pathogen. Molecular Plant Pathology 19:786-800.
Ray, S., and C. L. Casteel. 2022. Effector-mediated plant–virus–vector interactions. The Plant Cell 34(5):1514-1531. https://doi.org/10.1093/plcell/koac058 (accessed July 30, 2024).
Reitz, S. R., G. Maiorino, S. Olson, R. Sprenkel, A. Crescenzi, and M. T. Momol. 2008. Integrating plant essential oils and kaolin for the sustainable management of thrips and tomato spotted wilt on tomato. Plant Disease 92: 878-886.
Ricketts, K. D., M. I. Gomez, S. S. Atallah, M. F. Fuchs, T. E. Martinson, M. C. Battany, L. J. Bettiga, M. L. Cooper, P. S. Verdegaal, and R. J. Smith. 2015. Reducing the economic impact of grapevine leafroll disease in California: Identifying optimal disease management strategies. American Journal of Enology and Viticulture 66:138-147.
Ricketts, K. D., M. I. Gómez, M. F. Fuchs, T. E. Martinson, R. J. Smith, M. L. Cooper, M. M. Moyer, and A. Wise. 2017. Mitigating the economic impact of grapevine red blotch: Optimizing disease management strategies in U.S. vineyards. American Journal of Enology and Viticulture 68:127-135.
Roda, A., A. Francis, M. T. Kairo, and M. Culik. 2013. Planococcus minor (Hemiptera: Pseudococcidae): Bioecology, survey and mitigation strategies. In Potential invasive pests of agricultural crops, edited by J. Peña. Wallingford UK: CABI. Pp. 288-300.
Rong, W., J. Rollin, M. Hanafi, N. Roux, and S. Massart. 2023. Validation of high-throughput sequencing as virus indexing test for Musa germplasm: Performance criteria evaluation and contamination monitoring using an alien control. PhytoFrontiers 3:91-102.
Rosati, A. 2007. Physiological effects of kaolin particle film technology: A review. Functional Plant Science and Biotechnology 1:100-105. http://www.globalsciencebooks.info/Online/GSBOnline/images/0706/FPSB_1(1)/FPSB_1(1)100-105o.pdf (accessed July 29, 2024).
Roush, R. T., and G. L. Miller. 1986. Considerations for design of insecticide resistance monitoring programs. Journal of Economic Entomology 79:293-298.
Ruiz-Villalba, A., E. van Pelt-Verkuil, Q. D. Gunst, J. M. Ruijter, and M. J. van den Hoff. 2017. Amplification of nonspecific products in quantitative polymerase chain reactions (qPCR). Biomolecular Detection and Quantification 1(14):7-18.
Sáenz-Romo, M. G., A. Veas-Bernal, H. Martínez-García, R. Campos-Herrera, S. Ibáñez-Pascual, E. Martínez-Villar, I. Pérez-Moreno, and V. S. Marco-Mancebón. 2019. Ground cover management in a Mediterranean vineyard: Impact on insect abundance and diversity. Agriculture, Ecosystems & Environment 283:106571.
Sarkar, S. C., E. Wang, S. Wu, and Z. Lei. 2018. Application of trap cropping as companion plants for the management of agricultural pests: A review. Insects 9(4):128.
Scorza, R., A. Callahan, C. Dardick, M. Ravelonandro, J. Polak, T., Malinowski, I. Zagrai, M. Cambra, and I. Kamenova. 2013. Genetic engineering of plum pox virus resistance: ‘HoneySweet’ plum—from concept to product. Plant Cell, Tissue and Organ Culture 115:1-12.
Setiono, F., D. Chatterjee, M. Fuchs, K. L. Perry, and J. R. Thompson. 2018. The distribution and detection of grapevine red blotch virus in its host depend on time of sampling and tissue type. Plant Disease 102(11):2187-2193.
Shapira, I., T. Keasar, A. R. Harari, E. Gavish-Regev, M. Kishinevsky, H. Steinitz, C. Sofer-Arad, M. Tomer, A. Avraham, and R. Sharon. 2018. Does mating disruption of Planococcus ficus and Lobesia botrana affect the diversity, abundance and composition of natural enemies in Israeli vineyards? Pest Management Science 74(8):1837-1844.
Sharma, L., F. Gonçalves, I. Oliveira, L. Torres, and G. Marques. 2018. Insect-associated fungi from naturally mycosed vine mealybug Planococcus ficus (Signoret)(Hemiptera: Pseudococcidae). Biocontrol Science and Technology 28(2):122-141.
Sharon, R., T. Zahavi, T. Sokolsky, C. Sofer-Arad, M. Tomer, R. Kedoshim, and A. R. Harari. 2016. Mating disruption method against the vine mealybug, Planococcus ficus: Effect of sequential treatment on infested vines. Entomologia Experimentalis et Applicata 161(1):65-69.
Shelton, A. M., and F. R. Badenes-Perez. 2006. Concepts and applications of trap cropping in pest management. Annual Review of Entomology 51: 285-308.
Singerman, A., S. H. Lence, and P. Useche. 2017. Is area-wide pest management useful? The case of citrus greening. Applied Economic Perspectives and Policy 39:609-634.
Singh, N., and N. Gupta. 2017. Decision-making in integrated pest management and Bayesian network. International Journal of Computer Science & Information Technology 9(2):31-37.
Sisterson, M., and D. Stenger. 2012. Roguing with replacement in perennial crops: Conditions for successful disease management. Phytopathology 103(2):117-28.
Sisterson, M. S., D. P. Dwyer, and S. Y. Uchima. 2022. Evaluation of alfalfa fields and pastures as sources of Spissistilus festinus (Hemiptera: Membracidae): Quantification of reproductive and nutritional parameters. Environmental Entomology 52:119-128.
Soltani, N., K. A. Stevens, V. Klaassen, M.-S. Hwang, D. A. Golino, and M. Al Rwahnih. 2021. Quality assessment and validation of high-throughput sequencing for grapevine virus diagnostics. Viruses 13(6):1130. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8231206/ (accessed August 29, 2024).
Speirs, S., D. Reuter, K. Peverill, and R. Brennan. 2013. Making better fertiliser decisions for cropping systems in Australia: An overview. Crop and Pasture Science 64: 417–423.
Stillson, P. T., E. H. Bloom, J. G. Illán, and Z. Szendrei. 2020. A novel plant pathogen management tool for vector management. Pest Management Science 76:3729-3737.
Taber, M. R., and L. R. Martin. 1998. The use of netting as a bird management tool in vineyards. In Proceedings of the vertebrate pest conference 18(18), edited by R. O. Baker and A. C. Crabb. https://digitalcommons.unl.edu/cgi/viewcontent.cgi?httpsredir=1&article=1074&context=vpc18 (accessed August 20, 2024).
Tacoli, F., V. A. Bell, E. Cargnus, and F. Pavan. 2018. Insecticidal activity of natural products against vineyard mealybugs (Hemiptera: Pseudococcidae). Crop Protection 111:50-57.
Thompson, B. D., J. Dahan, J. Lee, R. R. Martin, and A. V. Karasev. 2019. A novel genetic variant of grapevine leafroll-associated virus-3 (GLRaV-3) from Idaho grapevines. Plant Disease 103(3):509-518.
Topuz, K., Davazdahemami, B., and D. A. Delen. 2023. A Bayesian belief network-based analytics methodology for early-stage risk detection of novel diseases. Annals of Operations Research 341:673-697.
Trichilo, P. J., and L. T. Wilson. 1993. An ecosystem analysis of spider mite outbreaks: Physiological stimulation or natural enemy suppression. Experimental and Applied Acarology 17:291-314.
Tricoli, D. 2024. Protoplast-mediated gene editing for disease resistance. Presentation at the National Academies of Sciences, Engineering, and Medicine Open Session, March 4, 2024.
Tricoll, D., K. Carney, P. Russell, J. R. MacMaster, D. W. Groff, K. C. Hadden, P. T. Himmel, J. P. Hubbard, M. L. Boeshore, and H. D. Quemada. 1995. Field evaluation of transgenic squash containing single or multiple virus coat protein gene constructs for resistance to cucumber mosaic virus, watermelon mosaic virus 2, and zucchini yellow mosaic virus. Nature Biotechnology 13:1458-1465.
Tripathi, S., J. Suzuki, and D. Gonsalves. 2007. Development of genetically engineered resistant papaya for papaya ringspot virus in a timely manner: A comprehensive and successful approach. Methods in Molecular Biology 354:197-240.
Tsai, C.-W., J. Chau, L. Fernandez, D. Bosco, K. M. Daane, and R. P. P. Almeida. 2008. Transmission of grapevine leafroll-associated virus 3 by the vine mealybug (Planococcus ficus). Phytopathology 98:1093-1098.
UC (University of California) IPM. n.d. Three cornered alfalfa hopper. Agriculture: Alfalfa pest management guidelines. https://ipm.ucanr.edu/agriculture/alfalfa/threecornered-alfalfahopper/#gsc.tab=0 (accessed September 3, 2024).
Van Timmeren, S., J. C. Wise, and R. Isaacs. 2012. Soil application of neonicotinoid insecticides for control of insect pests in wine grape vineyards. Pest Management Science 68:537-542.
Vashisth, T., Schumann, A. W., A. Singerman, A. L. Wright, R. S. Ferrarezi, J. Qureshi, and F. Alferez. 2021. 2021–2022 Florida citrus production guide: Citrus under protective screen (cups) production systems. Chapter 22, CMG19/HS1304, rev. 4/2021. EDIS 2021 (CPG). Gainesville, FL. https://doi.org/10.32473/edis-hs1304-2021.
Velásquez, A. C., C. D. M. Castroverde, and S. Y. He. 2018. Plant–pathogen warfare under changing climate conditions. Current Biology 28(10):R619-R634.
Venkatesan, T., S. K. Jalali, S. L. Ramya, and M. Prathibha. 2016. Insecticide resistance and its management in mealybugs. In Mealybugs and their management in agricultural and horticultural crops, edited by M. Mani and C. Shivaraju. New Delhi: Springer India. Pp. 223-229.
Vigne, E., A. Marmonier, V. Komar, O. Lemaire, and M. Fuchs. 2009. Genetic structure and variability of virus populations in cross-protected grapevines superinfected by Grapevine fanleaf virus. Virus Research 144(1-2):154-62.
Walker, A., and A. Tenscher. 2019. Breeding Pierce’s disease resistant winegrapes. Research progress reports: Pierce’s disease and other designated pests and diseases of winegrapes—December 2019. California Department of Food and Agriculture, Sacramento, CA. Pp. 104-115.
Walton, V. M., K. M. Daane, W. J. Bentley, J. G. Millar, T. E. Larsen, and R. Malakar-Kuenen. 2006. Pheromone-based mating disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in California vineyards. Journal of Economic Entomology 99(4):1280-1290.
Walton, V. M., A. J. Dreves, P. A. Skinkis, C. Kaiser, M. A. Buchanan, R. Hilton, B. Martin, S. Castagnoli, and S. B. Renquist. 2009. Grapevine leafroll virus and mealybug prevention and management in Oregon vineyards. EM 8990:1-4. Corvallis, OR: Oregon State University, https://ir.library.oregonstate.edu/downloads/fn106z37b (accessed July 31, 2024).
Wilson, H., K. M. Daane, R. J. Smith, and M. L. Cooper. n.d. Three-cornered alfalfa hopper (Spissistilus festinus) in vineyards. https://cenapa.ucanr.edu/newsletters/Vineyard_Views_Newsletter_-_Events86242.pdf (accessed July 31, 2024).
Wistrom, C., M. S. Sisterson, M. P. Pryor, J. M. Hashim-Buckey, and K. M. Daane. 2010. Distribution of glassy-winged sharpshooter and three-cornered alfalfa hopper on plant hosts in the San Joaquin Valley, California. Journal of Economic Entomology 103:1051-1059.
Wood, T. K. 1993. Diversity in the new world Membracidae. Annual Review of Entomology 38:409-433.
Xu, Q.-X., T.-W. Wang, C.-F. Cai, Z.-X. Li, Z.-H. Shi, and R.-J. Fang. 2013. Responses of runoff and soil erosion to vegetation removal and tillage on steep lands. Pedosphere 23:532-541.
Xu, X. J., Q. Zhu, S. Y. Jiang, Z. Y. Yan, C. Geng, Y. P. Tian, and X. D. Li. 2021. Development and evaluation of stable sugarcane mosaic virus mild mutants for cross-protection against infection by severe strain. Frontiers in Plant Science 12:788963, https://doi.org/10.3389/fpls.2021.788963/full (accessed July 31, 2024).
Yang, X., C. Nie, J. Zhang, H. Feng, and G. Yang. 2019. A Bayesian Network Model for Yellow Rust Forecasting in Winter Wheat. In Computer and computing technologies in agriculture XI. CCTA 2017. IFIP Advances in Information and Communication Technology, vol 545, edited by D. Li and C. Zhao. Springer, Cham. Pp. 65-75.
Yoon, J. Y., H. I. Ahn, M. Kim, S. Tsuda, and K. H. Ryu. 2006. Pepper mild mottle virus pathogenicity determinants and cross protection effect of attenuated mutants in pepper. Virus Research 118(1-2):23-30.
Zhang, X.-F., S. Zhang, Q. Guo, R. Sun, T. Wei, and F. Qu. 2018. A new mechanistic model for viral cross protection and superinfection exclusion. Frontiers in Plant Science 9:40.
Zhao, Y., X. Yang, G. Zhou, and T. Zhang. 2019. Engineering plant virus resistance: From RNA silencing to genome editing strategies. Plant Biotechnology Journal 18:328-336. https://doi.org/10.1111/pbi.13278 (accessed July 31, 2024).
Zhou, A., X. Qu, L. Shan, and X. Wang. 2017. Temperature warming strengthens the mutual-ism between ghost ants and invasive mealybugs. Scientific Reports 7:959.
