Sparganothis sulfureana (Lepidoptera: Tortricidae) egg surface characteristics stimulate parasitism by Ascogaster mimetica (Hymenoptera: Braconidae).

Ascogaster mimetica Viereck is an egg-larval parasitoid that targets Sparganothis sulfureana Clemens, a major cranberry pest in North America. While previous studies have shown that other Ascogaster species respond to cues from their hosts' eggs, it remains unknown whether A. mimetica utilizes these cues to recognize S. sulfureana. We hypothesized that female A. mimetica recognizes S. sulfureana from another cranberry pest, Choristoneura parallela Robinson, based on the presence of surface cues on eggs. To test this, we observed female A. mimetica behavior when exposed to eggs from its host, S. sulfureana; a nonhost, C. parallela; and eggs of S. sulfureana that were washed clean with hexane. Additionally, we tracked parasitism rates in each group. Our results revealed that A. mimetica spent 9.5 times longer walking when exposed to C. parallela eggs and 6 times longer when exposed to hexane-washed S. sulfureana eggs compared to unwashed S. sulfureana eggs. Also, A. mimetica spent 3 times longer grooming when exposed to hexane-washed than unwashed S. sulfureana eggs. In contrast, females spent 6 and 18 times longer drumming and probing/ovipositing on unwashed S. sulfureana eggs than on C. parallela eggs and 5 times longer probing/ovipositing on unwashed S. sulfureana eggs than on hexane-washed S. sulfureana eggs. Higher parasitism rates were observed from unwashed S. sulfureana eggs compared to those from C. parallela eggs and hexane-washed S. sulfureana eggs. Our findings suggest that the presence of egg surface cues, like scales, of S. sulfureana likely plays a crucial role in host acceptance and parasitism success for A. mimetica.

Phytoplasma infection renders cranberries more susceptible to above- and belowground insect herbivores.

While phytoplasma infections in plants are known to affect their interactions with aboveground herbivores, the impact of different genotypes on these infections and their effects on belowground herbivores remains largely unexplored. In cranberry (Vaccinium macrocarpon), infection by the phytoplasma Candidatus Phytoplasma sp. subgroup 16SrIII-Y leads to false blossom disease. This study investigates whether cranberry infection by this phytoplasma affects the performance and feeding behavior of a foliar feeder (spongy moth, Lymantria dispar) and a root feeder (oriental beetle, Anomala orientalis). Using phytoplasma-infected and uninfected cranberries of two genotypes ("Ben Lear" and "Crimson Queen"), the survival, growth and consumption of L. dispar and A. orientalis larvae were measured. To assess the effects on plant morphological and chemical traits, we also examined the impact of phytoplasma infection on shoot and root growth, carbon and nitrogen content, and the levels of defensive compounds such as proanthocyanidins (PACs). Results indicate that larvae of L. dispar and A. orientalis generally showed larger size and more efficient tissue consumption on infected plants, with these effects varying by cranberry genotype, possibly due to differences in phytoplasma titer. Phytoplasma infection was associated with stunted growth, elevated nitrogen content, and lower PAC levels in both shoots and roots of infected cranberry plants compared to uninfected ones. These findings indicate that phytoplasma infection potentially manipulates plant chemical composition by increasing nutrient levels and decreasing defensive compounds, enhancing herbivore performance both above and belowground. This study sheds light on the intricate interplay among plants, phytoplasma infection, and insect herbivore communities.

Genotypic Variation and Potential Mechanisms of Resistance against Multiple Insect Herbivores in Cranberries.

Plant genotypes often exhibit varying resistance levels to herbivores. However, the impact of this genotypic variation on resistance against multiple herbivores remains poorly understood, especially in crops undergoing recent process of domestication. To address this gap, we studied the magnitude and mechanism of resistance in 12 cranberry (Vaccinium macrocarpon) genotypes to three leaf-chewing herbivores - Sparganothis fruitworm (Sparganothis sulfureana), spotted fireworm (Choristoneura parallela), and spongy moth (Lymantria dispar) - along a domestication gradient (native 'wild' genotypes, 'early hybrid' genotypes, and 'modern hybrid' genotypes). Like cranberries, S. sulfureana and C. parallela are native to the United Sates, while L. dispar is an invasive pest. We measured the survival and growth of larvae on each genotype, as well as variation in plant performance (height and biomass) and leaf defensive chemical traits (C/N ratio, total phenolics, total proanthocyanidins, and flavonols levels) in these genotypes to elucidate potential resistance mechanisms. We found differences in C. parallela and L. dispar larval performance across genotypes, with larvae performing better on the modern hybrid genotypes, while S. sulfureana showed no differences. Morphological and chemical traits varied among genotypes, with total phenolics being the only trait correlated with C. parallela and L. dispar larval performance. Notably, the wild genotypes 'McFarlin' and 'Potter' had higher total phenolics and were more resistant to both herbivores than the modern hybrids 'Demoranville' and 'Mullica Queen.' This research contributes to a comprehensive understanding of the impact of crop domestication on multiple insect herbivores, offering insights for future breeding efforts to enhance host-plant resistance against agricultural pests.

Testing the Effects of Prey Type on the Life History and Population-Level Parameters of Chrysoperla externa (Neuroptera: Chrysopidae).

Green lacewings are valuable predators, utilized in augmentative biological control against various agricultural pests. However, further studies are required to comprehend the performance of these predators when consuming natural prey. We investigated the capacity of Chrysoperla externa (Hagen) to utilize the following three distinct prey types: the pupae of the coffee leaf miner Leucoptera coffeella (Guérin-Mèneville & Perrottet), the eggs of the sugarcane borer Diatraea saccharalis (F.), and the eggs of the Mediterranean flour moth Ephestia kuehniella (Zeller). The first two of these species are naturally occurring prey found in field crops, while the last serves as a factitious prey species for the mass rearing of natural enemies. We hypothesized that the type of prey would differentially affect the life history and population-level parameters of C. externa. Laboratory experiments were conducted to compare the pre-imaginal survival and developmental times, adult longevity and reproduction, and population growth of C. externa when larvae were provided with each of the three prey items. Results indicated that C. externa utilized the two natural prey items, L. coffeella pupae and D. saccharalis eggs, for its development, reproduction, and population growth. However, larvae developed significantly faster and females exhibited higher reproductive parameters, including fecundity and daily oviposition, when consuming the factitious prey, E. kuehniella eggs. This resulted in a higher intrinsic rate of population increase, as well as shorter times for the population to double in size. Understanding the population dynamics of C. externa when consuming different prey items is crucial for optimizing their utilization in augmentative biological control programs.

A theoretical framework to improve the adoption of green Integrated Pest Management tactics.

Sustainable agriculture relies on implementing effective, eco-friendly crop protection strategies. However, the adoption of these green tactics by growers is limited by their high costs resulting from the insufficient integration of various components of Integrated Pest Management (IPM). In response, we propose a framework within IPM termed Multi-Dimensional Management of Multiple Pests (3MP). Within this framework, a spatial dimension considers the interactive effects of soil-crop-pest-natural enemy networks on pest prevalence, while a time dimension addresses pest interactions over the crop season. The 3MP framework aims to bolster the adoption of green IPM tactics, thereby extending environmental benefits beyond crop protection.

Evaluation of a Push-Pull Strategy for Spotted-Wing Drosophila Management in Highbush Blueberry.

We evaluated a novel push-pull control strategy for protecting highbush blueberry, Vaccinium corymbosum, against spotted-wing drosophila (SWD), Drosophila suzukii. Methyl benzoate (MB) was used as the pushing agent and a previously tested SWD attractive blend of lure-scents was used as the pulling agent. MB dispensers (push) were hung in the canopy and lure-scent dispensers (pull) were hung in yellow jacket traps filled with soapy water around the blueberry bushes. Blueberries were sampled weekly, and any infestation was inspected by examining the breathing tubes of SWD eggs which protrude through the skin of infested fruit. The frequency of infestation, i.e., the proportion of berries infested with at least one egg, and the extent of infestation, i.e., the mean number of eggs in infested berries, were significantly reduced in treatments receiving MB dispensers as a pushing agent when infestation rates were very high. However, the mass trapping devices as a pulling agent did not provide comparable protection on their own and did not produce additive protection when used in combination with the MB dispensers in push-pull trials. We conclude that MB has the potential to be implemented as a spatial repellent/oviposition deterrent to reduce SWD damage in blueberry under field conditions and does not require the SWD attractant as a pulling agent to achieve crop protection.

An insect's energy bar: the potential role of plant guttation on biological control.

Plant guttation is an exudation fluid composed of xylem and phloem sap secreted at the margins of leaves of many agricultural crops. Although plant guttation is a widespread phenomenon, its effect on natural enemies remains largely unexplored. A recent study showed that plant guttation can be a reliable nutrient-rich food source for natural enemies, affecting their communities in highbush blueberries. This review highlights the potential role of plant guttation as a food source for natural enemies, with a particular emphasis on its nutritional value, effects on insect communities, and potential use in conservation biological control. We also discuss possible negative implications and conclude with some open questions and future directions for research.

Comparison of multimodal attract-and-kill formulations for managing Drosophila suzukii: Behavioral and lethal effects.

Attract-and-kill (A&K) is a potential alternative control tactic for managing the invasive spotted-wing drosophila, Drosophila suzukii Matsumura. Here, we compared the efficacy of two novel A&K formulations based on proprietary blends-ACTTRA SWD OR1 (henceforth OR1) and ACTTRA SWD TD (henceforth TD)-in managing D. suzukii. Using two-choice bioassays, we compared OR1 and TD for their relative attractiveness to adult D. suzukii. Additionally, we tested how the addition of (1) a red dye (visual cue) and (2) the insecticide spinosad (Entrust™) to the OR1 and TD formulations influenced the attraction of adult D. suzukii in the presence of blueberry fruits. Finally, complementary laboratory efficacy (no-choice) bioassays were conducted to assess the mortality of adult D. suzukii exposed to OR1 and TD. A direct comparison between TD and OR1 formulations indicated the TD formulation was ~8 times more attractive than OR1. Adding a red dye to the TD or OR1 formulation did not significantly alter the attraction or mortality of adult D. suzukii compared to the formulation without a dye. Similarly, irrespective of dye status, adding spinosad to either the TD or OR1 formulation did not alter the adult D. suzukii behavioral response to these formulations but resulted in significantly higher D. suzukii mortality. Overall, the TD formulations resulted in significantly higher, or at least comparable, mortality to the OR1 formulations. In summary, our laboratory results demonstrated the higher efficacy of a TD-based A&K product in managing D. suzukii over its well-tested predecessor, the OR1 formulation, confirming its potential as a new behavioral tactic against this pest.

Blueberries infected with the fungal pathogen Colletotrichum fioriniae release odors that repel Drosophila suzukii.

BACKGROUND: Spotted-wing drosophila, Drosophila suzukii, is a serious pest of thin-skinned fruits. Alternative methods to control this pest are needed to reduce insecticide use, including new repellents. Previous research demonstrated that D. suzukii adults use odor cues to avoid blueberries infected with the fungal pathogen Colletotrichum fioriniae, which causes the disease anthracnose. To identify novel D. suzukii repellents, we investigated the volatile emission from experimentally-infected fruit, which were inoculated with C. fioriniae isolates in the laboratory, and from field-collected fruit, which were naturally infected and harvested from a field. We then tested the pathogen-induced volatiles on D. suzukii adult behavior. RESULTS: Volatile emission was similar between all five C. fioriniae strains, with good agreement between experimentally-infected and field-collected berries. In total, 14 volatiles were found to be more abundant in infected versus uninfected fruit headspace. In multiple-choice bioassays, nine of the 14 volatiles elicited repellency responses from adult D. suzukii. These nine volatiles were further evaluated in dual choice assays, where all nine reduced fly capture by 43-96% compared to the control. The most repellent compounds tested were the esters ethyl butanoate and ethyl (E)-but-2-enoate, which were more or equally repellent to the known D. suzukii repellents 1-octen-3-ol, geosmin, and 2-pentylfuran. Dose-response assays identified concentration-dependent effects on D. suzukii repellency and oviposition when applied individually and consistent aversion observed across doses of a 1:1 blend. CONCLUSION: We report two repellents from C. fioriniae-infected blueberries that could be useful semiochemicals for the behavioral manipulation of D. suzukii in the field. © 2023 Society of Chemical Industry. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Functional response of 3 green lacewing species (Neuroptera: Chrysopidae) to Leucoptera coffeella (Lepidoptera: Lyonetiidae).

Green lacewings (Neuroptera: Chrysopidae) are predators commonly found in coffee plantations in Brazil that can serve as important biological control agents against insect pests such as the coffee leaf miner, Leucoptera coffeella (Lepidoptera: Lyonetiidae). However, the efficacy of different lacewing species in controlling L. coffeella needs to be evaluated before they are used in augmentative biological control programs. Here, laboratory experiments were conducted to investigate the effects of the L. coffeella developmental stage on the functional response of 3 species of green lacewings: Chrysoperla externa, Ceraeochrysa cincta, and Ceraeochrysa cornuta. The attack rate, handling time, and the number of prey attacked during 24 h with different densities (1, 2, 4, 8, 16, 32, and 64 individuals) of either L. coffeella larvae or pupae were recorded for each of the 3 lacewing species. Based on logistic regression models, all 3 predators showed a Type II functional response when consuming both larvae and pupae of L. coffeella. All 3 species also had similar attack rates (0.0091 larva/h and 0.0095 pupa/h), handling times (3.5 and 3.7 h for larvae and pupae, respectively), and estimated number of prey attacked during the observation period (6.9 larvae and 6.6 pupae) for L. coffeella larvae and pupae. Therefore, our laboratory studies show that the 3 green lacewings Ch. externa, Ce. cincta, and Ce. cornuta have potential for the biological control of L. coffeella, although these results need to be confirmed under field conditions. These findings have implications for the selection of lacewings for augmentative L. coffeella biocontrol.

The contrasting role of climate variation on the population dynamics of a native and an invasive insect pest.

Since 2008, spotted-wing drosophila, Drosophila suzukii, has become a major pest of soft, thin-skinned fruits in the USA, causing significant annual yield losses. Historically, the native blueberry maggot fly, Rhagoletis mendax, has been a key blueberry pest in eastern North America and a driver of insecticide usage. After its invasion in 2011 into New Jersey (USA), D. suzukii has supplanted R. mendax as the main target of insecticide applications in the state. However, the impact of D. suzukii on the native R. mendax has not been documented, particularly in relation to local climate. Historical monitoring data from New Jersey blueberry farms were used to assess the role of climate on R. mendax and D. suzukii populations. Seasonal trap captures of R. mendax adults have decreased after D. suzukii invasion, while D. suzukii trap captures have increased. Similarly, D. suzukii first captures have occurred earlier each year, while R. mendax has been captured later in the growing season. Winter freezing and summer growing degree days were found to significantly correlate with D. suzukii activity. Using downscaled climate simulations, we projected that D. suzukii will arrive in New Jersey blueberry fields up to 5 days earlier on average by 2030 and 2 weeks earlier by 2050 with warming temperatures, exacerbating yield losses and insecticide usage. As regional temperatures are projected to warm and the invasive range continues to expand, we predict the rate of phenological development of the invasive D. suzukii and its impact on native insects to change noticeably, bringing new challenges for pest management strategies.

Using Red Panel Traps to Detect Spotted-Wing Drosophila and its Infestation in US Berry and Cherry Crops.

Spotted-wing drosophila (SWD), Drosophila suzukii Matsumura (Diptera: Drosophilidae), is an invasive pest of thin-skinned fruits in the United States. Monitoring traps are an integral part of SWD integrated pest management, allowing early detection and timely management of this pest. An ideal monitoring trap should be easy to use, effective in capturing SWD, sensitive and selective to male SWD which are easy to identify due to their spotted wings, and able to predict fruit infestation from trap captures. Deli-cup-based liquid traps (grower standard), which make in-situ observations difficult, were compared with red-panel sticky traps, both baited with commercial lures (Scentry, Trécé Broad-Spectrum (BS), and Trécé High-Specificity (HS)), across several US states in blueberries (lowbush and highbush), blackberry, raspberry, and cherry crops during 2018 and 2021. Results showed that red-panel traps effectively captured SWD, were able to detect male SWD early in the season while also being selective to male SWD all season-long, and in some cases linearly related male SWD trap captures with fruit infestation. Scentry and Trécé BS lures captured similar numbers of SWD, though Trécé BS and Trécé HS were more selective for male SWD in red panel traps than liquid traps in some cases. In conclusion, due to its ease of use with less processing time, red-panel traps are promising tools for detecting and identifying male SWD in-situ and for predicting fruit infestation. However, further research is needed to refine the trap captures and fruit infestation relationship and elucidate the trap-lure interactions in berry and cherry crops.

Population Genetics of the Blueberry Gall Midge, Dasineura oxycoccana (Diptera: Cecidomyiidae), on Blueberry and Cranberry and Testing Invasion Scenarios.

We compared the population genetic structure between populations of the blueberry gall midge-Dasineura oxycoccana (Johnson) (Diptera: Cecidomyiidae)-from blueberry and cranberry and determined the genetic relationships among geographical subgroups by genotyping 632 individuals from 31 different populations from their native USA regions (New Jersey, Michigan, and Georgia) and from invaded Korean regions using 12 microsatellite loci. Our population genetic analyses showed a clear separation between the two host-associated D. oxycoccana populations from blueberry and cranberry. Using data from only the blueberry-associated D. oxycoccana populations, we identified five genetically isolated subgroups. An analysis of the approximate Bayesian computation suggests that the invasive D. oxycoccana population from Korea appears to have been introduced from an unsampled source population rather than directly from its native range. Our findings will allow for an easier identification of the source of D. oxycoccana into newly invaded regions, as well as to determine their association with blueberry and cranberry, which based on our results can be considered as two distinct species.

Molecular and behavioral studies reveal differences in olfaction between winter and summer morphs of Drosophila suzukii.

Spotted-wing drosophila, Drosophila suzukii (Matsumura), is a major economic pest of several fruit crops in Europe, North and South America, and other parts of the world because it oviposits in ripening thin-skinned fruits. This vinegar fly exhibits two distinct morphotypes: a summer and a winter morph. Although adaptations associated with the winter morph enhance this invasive pest's capacity to survive in cold climates, winter is still a natural population bottleneck. Since monitoring early spring populations is important for accurate population forecasts, understanding the winter morph's response to olfactory cues may improve current D. suzukii management programs. In this study, a comparative transcriptome analysis was conducted to assess gene expression differences between the female heads of the two D. suzukii morphs, which showed significant differences in 738 genes (p ≤ 0.0001). Out of twelve genes related to olfaction determined to be differentially expressed in the transcriptome, i.e., those related to location of food sources, chemosensory abilities, and mating behavior, nine genes were upregulated in the winter morph while three were downregulated. Three candidate olfactory-related genes that were most upregulated or downregulated in the winter morph were further validated using RT-qPCR. In addition, behavioral assays were performed at a range of temperatures to confirm a differing behavioral response of the two morphs to food odors. Our behavioral assays showed that, although winter morphs were more active at lower temperatures, the summer morphs were generally more attracted to food odors. This study provides new insights into the molecular and behavioral differences in response to olfactory cues between the two D. suzukii morphs that will assist in formulating more effective monitoring and physiological-based control tools.

Novel hosts can incur fitness costs to a frugivorous insect pest.

In phytophagous insects, adult attraction and oviposition preference for a host plant are often positively correlated with their immature fitness; however, little is known how this preference-performance relationship changes within insect populations utilizing different host plants. Here, we investigated differences in the preference and performance of two populations of a native North American frugivorous insect pest, the plum curculio (Conotrachelus nenuphar)-one that utilizes peaches and another that utilizes blueberries as hosts-in the Mid-Atlantic United States. We collected C. nenuphar adult populations from peach and blueberry farms and found that they exhibited a clear preference for the odors of, as well as an ovipositional preference for, the hosts they were collected from, laying 67%-83% of their eggs in their respective collected hosts. To measure C. nenuphar larval performance, a fitness index was calculated using data on larval weights, development, and survival rate from egg to 4th instars when reared on the parent's collected and novel hosts. Larvae of C. nenuphar adults collected from peach had high fitness on peach but low fitness when reared on blueberry. In contrast, larvae from C. nenuphar adults collected in blueberry had high fitness regardless of the host on which they were reared. In this study, we show that utilizing a novel host such as blueberry incurs a fitness cost for C. nenuphar from peaches, but this cost was not observed for C. nenuphar from blueberries, indicating that the preference-performance relationship is present in the case of insects reared on peach, but insects reared on blueberry were more flexible and able to utilize either host, despite preferring blueberry.

Monitoring of Spotted-Wing Drosophila (Diptera: Drosophilidae) Resistance Status Using a RAPID Method for Assessing Insecticide Sensitivity Across the United States.

Drosophila suzukii (Matsumura) has spread rapidly, challenging berry and cherry crop production due to its ability to lay eggs into ripening fruit. To prevent infestation by this pest, insecticides are applied during fruit ripening and harvest. We field-tested the Rapid Assessment Protocol for IDentification of resistance in D. suzukii (RAPID) on seventy-eight populations collected across eight U.S. states in 2017 and 2018. Exposure to LC50 rates of malathion, methomyl, spinetoram, spinosad, and zeta-cypermethrin led to average female fly mortality of 25.0% in 2017, and after adjusting concentrations the average was 39.9% in 2018. Using LC99 × 2 discriminating concentrations in 2017 and LC90 × 8 rates in 2018, average female mortalities were 93.3% and 98.5%, respectively, indicating high overall susceptibility. However, using these high concentrations we found 32.0% of assays with survival of some female flies in 2017 and 27.8% in 2018. The adjustment in discriminating dose from 2017 to 2018 also reduced the proportion of assays with <90% survival from 17.6 to 2.9%. Populations with low mortality when exposed to spinosad were identified using this assay, triggering more detailed follow-up bioassays that identified resistant populations collected in California coastal region berry crops. Widespread evaluations of this method and subsequent validation in California, Michigan, and Georgia in 2019-2021 show that it provides a quick and low-cost method to identify populations of D. suzukii that warrant more detailed testing. Our results also provide evidence that important insecticide classes remain effective in most U.S. regions of fruit production.

Factors Influencing the Efficacy of Novel Attract-and-Kill (ACTTRA SWD) Formulations Against Drosophila suzukii.

In the continental United States, the invasive spotted-wing drosophila (SWD), Drosophila suzukii Matsumura, has become a primary pest of multiple stone and soft-skinned fruits. A new innovative adjuvant formulation, ACTTRA SWD, mixed with a suitable insecticide, constitutes a novel attract-and-kill tactic to manage D. suzukii in fruit crops. We hypothesized that background odors present in crop fields, particularly odors from host fruits, negatively affect the effectiveness of this attract-and-kill formulation, as odors from these sources can compete for insect attraction. Additionally, we evaluated the influence of adult D. suzukii sex and physiological status (age and mating status), and fruit ripeness on its response to the ACTTRA SWD formulation. For this, we used two-choice bioassays to test the response of adult D. suzukii to three ACTTRA SWD formulations (named OR1, TD, and HOOK SWD) in the presence and absence of host fruits (blueberries, raspberries, blackberries, and strawberries). Odors from raspberries were significantly more attractive than those from the TD formulation mixed with spinosad (Entrust). For the HOOK SWD formulation and OR1+Entrust formulation, odors from all the fruit types tested were significantly more attractive than the adjuvants. Compared with females, male D. suzukii were more attracted to the TD formulation over the blueberry fruits. Additionally, age and female mating status but not fruit ripeness influenced D. suzukii attraction to both OR1 and TD formulations. The results from this study indicate that D. suzukii physiological status and host fruit availability impact the efficacy of new attract-and-kill adjuvants such as ACTTRA SWD.

Bottom-Up Forces in Agroecosystems and Their Potential Impact on Arthropod Pest Management.

Bottom-up effects are major ecological forces in crop-arthropod pest-natural enemy multitrophic interactions. Over the past two decades, bottom-up effects have been considered key levers for optimizing integrated pest management (IPM). Irrigation, fertilization, crop resistance, habitat manipulation, organic management practices, and landscape characteristics have all been shown to trigger marked bottom-up effects and thus impact pest management. In this review, we summarize current knowledge on the role of bottom-up effects in pest management and the associated mechanisms, and discuss several key study cases showing how bottom-up effects practically promote natural pest control. Bottom-up effects on IPM also contribute to sustainable intensification of agriculture in the context of agricultural transition and climate change. Finally, we highlight new research priorities in this important area. Together with top-down forces (biological control), future advances in understanding ecological mechanisms underlying key bottom-up forces could pave the way for developing novel pest management strategies and new optimized IPM programs.