Transgenerational effects of grandparental and parental diets combine with early-life learning to shape adaptive foraging phenotypes in Amblyseius swirskii.

Transgenerational effects abound in animals. While a great deal of research has been dedicated to the effects of maternal stressors such as diet deficiency, social deprivation or predation risk on offspring phenotypes, we have a poor understanding of the adaptive value of transgenerational effects spanning across multiple generations under benign conditions and the relative weight of multigenerational effects. Here we show that grandparental and parental diet experiences combine with personal early-life learning to form adaptive foraging phenotypes in adult plant-inhabiting predatory mites Amblyseius swirskii. Our findings provide insights into transgenerational plasticity caused by persistent versus varying conditions in multiple ancestral generations and show that transgenerational effects may be adaptive in non-matching ancestor and offspring environments.

Population genomics of Drosophila suzukii reveal longitudinal population structure and signals of migrations in and out of the continental United States.

Drosophila suzukii, or spotted-wing drosophila, is now an established pest in many parts of the world, causing significant damage to numerous fruit crop industries. Native to East Asia, D. suzukii infestations started in the United States a decade ago, occupying a wide range of climates. To better understand invasion ecology of this pest, knowledge of past migration events, population structure, and genetic diversity is needed. In this study, we sequenced whole genomes of 237 individual flies collected across the continental United States, as well as several sites in Europe, Brazil, and Asia, to identify and analyze hundreds of thousands of genetic markers. We observed strong population structure between Western and Eastern US populations, but no evidence of any population structure between different latitudes within the continental United States, suggesting that there are no broad-scale adaptations occurring in response to differences in winter climates. We detect admixture from Hawaii to the Western United States and from the Eastern United States to Europe, in agreement with previously identified introduction routes inferred from microsatellite analysis. We also detect potential signals of admixture from the Western United States back to Asia, which could have important implications for shipping and quarantine policies for exported agriculture. We anticipate this large genomic dataset will spur future research into the genomic adaptations underlying D. suzukii pest activity and development of novel control methods for this agricultural pest.

Drosophila suzukii (Diptera: Drosophilidae): A Decade of Research Towards a Sustainable Integrated Pest Management Program.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) also known as spotted-wing drosophila (SWD), is a pest native to Southeast Asia. In the last few decades, the pest has expanded its range to affect all major European and American fruit production regions. SWD is a highly adaptive insect that is able to disperse, survive, and flourish under a range of environmental conditions. Infestation by SWD generates both direct and indirect economic impacts through yield losses, shorter shelf life of infested fruit, and increased production costs. Fresh markets, frozen berries, and fruit export programs have been impacted by the pest due to zero tolerance for fruit infestation. As SWD control programs rely heavily on insecticides, exceedance of maximum residue levels (MRLs) has also resulted in crop rejections. The economic impact of SWD has been particularly severe for organic operations, mainly due to the limited availability of effective insecticides. Integrated pest management (IPM) of SWD could significantly reduce chemical inputs but would require substantial changes to horticultural management practices. This review evaluates the most promising methods studied as part of an IPM strategy against SWD across the world. For each of the considered techniques, the effectiveness, impact, sustainability, and stage of development are discussed.

Cultural Control of Drosophila suzukii in Small Fruit-Current and Pending Tactics in the U.S.

Spotted-wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), a vinegar fly of Asian origin, has emerged as a devastating pest of small and stone fruits throughout the United States. Tolerance for larvae is extremely low in fresh market fruit, and management is primarily achieved through repeated applications of broad-spectrum insecticides. These applications are neither economically nor environmentally sustainable, and can limit markets due to insecticide residue restrictions, cause outbreaks of secondary pests, and select for insecticide resistance. Sustainable integrated pest management programs include cultural control tactics and various nonchemical approaches for reducing pest populations that may be useful for managing D. suzukii. This review describes the current state of knowledge and implementation for different cultural controls including preventative tactics such as crop selection and exclusion as well as strategies to reduce habitat favorability (pruning; mulching; irrigation), alter resource availability (harvest frequency; sanitation), and lower suitability of fruit postharvest (cooling; irradiation). Because climate, horticultural practices, crop, and market underlie the efficacy, feasibility, and affordability of cultural control tactics, the potential of these tactics for D. suzukii management is discussed across different production systems.

Mulching as a cultural control strategy for Drosophila suzukii in blueberry.

BACKGROUND: Fruit growers largely depend on chemical control to reduce populations of the economically damaging invasive fly, Drosophila suzukii (Matsumura). Drosophila suzukii is susceptible to high temperatures and low humidity; therefore, it may be possible to implement cultural control practices that create microclimates unfavorable for its development and survival. In addition to other fruit production benefits, in-row mulches may impede the development of D. suzukii immatures when larvae leave the fruit to pupate in the soil. This study compared the effects of different mulches (black polypropylene fabric weedmats, sawdust, and wood chips) on temperature and relative humidity (RH), and on adult emergence of D. suzukii from larvae in blueberries and pupae, both above and below the ground surface in blueberry plantings (Vaccinium corymbosum L.). RESULTS: Across regions, both lower larval survival and longer periods with high suboptimal temperatures occurred above the ground in comparison to buried below the ground, regardless of mulch type. Fewer D. suzukii adults emerged from larvae on weedmat mulch at one site, but there was no effect of mulch type on temperature, RH, or D. suzukii emergence at most sites. The relationships between temperature, RH, and the emergence of adults from larvae and pupae varied by region. Natural infestation by D. suzukii in blueberries was lower over weedmat compared to wood-based mulches at one site. Greenhouse experiments showed that larvae burrowed to pupate underneath sawdust mulch, but were unable to pupate underneath a weedmat mulch. CONCLUSIONS: Although weedmats may not modify temperatures or RH enough to consistently affect D. suzukii emergence, they can reduce field suitability for D. suzukii by providing a barrier that prevents larvae from reaching favorable pupation microhabitats underground. © 2019 Society of Chemical Industry.

Interactions among morphotype, nutrition, and temperature impact fitness of an invasive fly.

Invasive animals depend on finding a balanced nutritional intake to colonize, survive, and reproduce in new environments. This can be especially challenging during situations of fluctuating cold temperatures and food scarcity, but phenotypic plasticity may offer an adaptive advantage during these periods. We examined how lifespan, fecundity, pre-oviposition periods, and body nutrient contents were affected by dietary protein and carbohydrate (P:C) ratios at variable low temperatures in two morphs (winter morphs WM and summer morphs SM) of an invasive fly, Drosophila suzukii. The experimental conditions simulated early spring after overwintering and autumn, crucial periods for survival. At lower temperatures, post-overwintering WM lived longer on carbohydrate-only diets and had higher fecundity on low-protein diets, but there was no difference in lifespan or fecundity among diets for SM. As temperatures increased, low-protein diets resulted in higher fecundity without compromising lifespan, while high-protein diets reduced lifespan and fecundity for both WM and SM. Both SM and WM receiving high-protein diets had lower sugar, lipid, and glycogen (but similar protein) body contents compared to flies receiving low-protein and carbohydrate-only diets. This suggests that flies spend energy excreting excess dietary protein, thereby affecting lifespan and fecundity. Despite having to recover from nutrient depletion after an overwintering period, WM exhibited longer lifespan and higher fecundity than SM in favorable diets and temperatures. WM exposed to favorable low-protein diet had higher body sugar, lipid, and protein body contents than SM, which is possibly linked to better performance. Although protein is essential for oogenesis, WM and SM flies receiving low-protein diets did not have shorter pre-oviposition periods compared to flies on carbohydrate-only diets. Finding adequate carbohydrate sources to compensate protein intake is essential for the successful persistence of D. suzukii WM and SM populations during suboptimal temperatures.

Host and Non-host 'Whistle Stops' for Psyllids: Molecular Gut Content Analysis by High-Throughput Sequencing Reveals Landscape-Level Movements of Psylloidea (Hemiptera).

Psyllids (Hemiptera: Psylloidea) are phloem-feeding insects that tend to be highly specific in their host plants. Some species are well-known agricultural pests, often as vectors of plant pathogens. Many pest psyllids colonize agricultural fields from non-crop reproductive hosts or from non-host transitory and winter shelter plants. Uncertainty about which non-crop species serve as sources of psyllids hinders efforts to predict which fields or orchards are at greater risk of being colonized by psyllids. High-throughput sequencing of trnL, trnF, and ITS was used to examine the dietary histories of three pest and two non-pest psyllid species encompassing a diversity of lifecycles: Cacopsylla pyricola (Förster) (Psyllidae), Bactericera cockerelli (Sulc) (Triozidae), Diaphorina citri Kuwayama (Liviidae), Aphalara loca Caldwell (Aphalaridae), and a Cacopsylla species complex associated with Salix (Malphighiales: Salicaceae). Results revealed an unexpectedly high level of feeding on non-host species by all five psyllid species. The identification of the dietary history of the psyllids allowed us to infer their landscape-scale movements prior to capture. Our study demonstrates a novel use for gut content analysis-to provide insight into landscape-scale movements of psyllids-thus providing a means to pinpoint the non-crop sources of pest psyllids colonizing agricultural crops. We observed previously unknown psyllid behaviors during our efforts to develop this method and discuss new research directions for the study of psyllid ecology.

Does prey encounter and nutrient content affect prey selection in wolf spiders inhabiting Bt cotton fields?

Wolf spiders are abundant and voracious predators at the soil-plant interface in cotton crops. Among other prey, they attack late-instar larvae of the cotton bollworm Helicoverpa spp., an economically important pest. Consequently, wolf spiders in transgenic Bt cotton could provide significant biological control of Bt-resistant Helicoverpa larvae that descend to the soil to pupate. The predator-prey interactions between wolf spiders and Helicoverpa could, however, be constrained by the presence of alternative prey and intraguild predators. This study used laboratory enclosures to analyse the effect of alternative prey on predatory selection of the wolf spider Tasmanicosa leuckartii Thorell. The prey included another wolf spider Hogna crispipes Koch (potential intraguild predator), the ground cricket Teleogryllus commodus Walker (minor pest), and Helicoverpa armigera larvae (major pest). We tested if encounter rates, prey vulnerability, and prey nutritional content influenced the likelihood that a prey was attacked. In three-way food webs, Tasmanicosa encountered and attacked Teleogryllus and Helicoverpa in similar frequencies. However, in the presence of a competing intraguild predator and potential prey (Hogna) in a four-way food web, Tasmanicosa did not always attack Teleogryllus at first encounter, but still attacked Helicoverpa at each encounter. Helicoverpa (protein-poor) and Hogna (protein-rich) were consumed by Tasmanicosa in similar proportions, suggesting that Tasmanicosa might benefit from nutrient balance as an outcome of diverse prey in this food web. As Teleogryllus (protein rich) escapes quicker than Helicoverpa and Hogna, Hogna may be an easier protein-rich option than Teleogryllus. Field surveys showed that while Teleogryllus was the most common prey, wolf spiders feed on diverse insect taxa, as well as other spiders. That Tasmanicosa readily attacked Helicoverpa larvae in the presence of alternative prey is an encouraging result that supports the potential of Tasmanicosa predation to assist in the control of Bt-resistant Helicoverpa larvae and thereby inhibit the proliferation and spread of resistance.

Interactions Between Biotic and Abiotic Factors Affect Survival in Overwintering Drosophila suzukii (Diptera: Drosophilidae).

Drosophila suzukii Matsumura is an invasive species affecting berry crops and cherries throughout North America, South America, and Europe. Previous research suggests that in temperate climates, the overwintering success of D. suzukii is likely dependent on access to food, shelter, and adequate cold hardening. We performed a multi-state study under field conditions for two winters to determine whether D. suzukii sex, phenotype (summer-morphotype, winter-morphotype), and life stage (adults, pupae) affected survival over time while recording naturally-occurring spatial and temporal variation in temperature. Access to food was provided and the flies were buried under leaf litter. Baited traps were deployed to determine whether local populations of D. suzukii were active throughout the winter season. The duration of exposure, mean daily temperature, and cumulative time below freezing significantly affected survival. Below freezing, D. suzukii survival was significantly reduced, particularly in northern locations. In contrast, we observed sustained survival up to 10 wk in southern locations among adults and pupae. Biotic factors also significantly affected survival outcomes: female survival was greater than male survival, winter-morphotype survival was greater than summer-morphotype survival, and adult survival was greater than pupal survival. In the north, wild D. suzukii were captured only in early winter, while in the south they were found throughout the winter. These data suggest that although adult D. suzukii may overwinter in sheltered microclimates, this ability may be limited in regions where the ground temperature, or site of overwintering, falls below freezing for extended durations.

Drip and Overhead Sprinkler Irrigation in Blueberry as Cultural Control for Drosophila suzukii (Diptera: Drosophilidae) in Northwestern United States.

Overhead sprinkler compared to drip irrigation in cropping systems can result in increased relative humidity (RH) and decreased temperature within the plant canopy. Such conditions may also result in a more favorable microclimate for pests. Drosophila suzukii Matsumura is an invasive agricultural pest of berries in America and Europe. Drosophila suzukii is susceptible to high temperatures and low RH, thus its survival may be affected by different irrigation methods. We tested how drip and overhead sprinkler irrigation in blueberries influenced temperature and RH. Furthermore, we determined how these environmental factors affected adult emergence rates from larvae within fruit or pupae outside of fruit. RH was higher in overhead sprinkler compared to drip irrigation treatments, but there was no difference in temperatures. Although there were no differences in fly emergence from larvae between irrigation treatments, more flies emerged from pupae in overhead sprinkler compared to drip irrigation treatments. This is likely because larvae developing inside fruit are protected from desiccation, while pupae were exposed to lower RH. Regardless of irrigation method, temperatures remained above 30°C for longer periods and RH was lower above as opposed to below the mulch. Fewer D. suzukii larvae and pupae consequently survived above the mulch than below the mulch. When assessing natural infestation, we found similar numbers of D. suzukii flies emerging from blueberries collected on drip and sprinkler rows. Irrigation management can be coupled with other cultural control methods that ensure that pupae remain exposed on low RH surfaces, where they are more likely to succumb to desiccation.

Survival and Fecundity Parameters of Two Drosophila suzukii (Diptera: Drosophilidae) Morphs on Variable Diet Under Suboptimal Temperatures.

Life history parameters are used to estimate population dynamics, mortality, and reproduction in insects relative to their surrounding environment. For Drosophila suzukii Matsumura (Diptera: Drosophilidae), an invasive agricultural pest, previous studies have estimated net reproductive rate (Ro), generation time (T), and intrinsic rate of population increase (rm). A main limitation is that these estimates were measured under relatively favorable settings, and do not reflect environmental conditions and physiological states encountered during dormancy periods. Therefore, this study investigated the impacts of 1) low temperatures and 2) dietary protein: carbohydrate ratios (P:C) on both survival and fecundity parameters of D. suzukii summer morphs (SM) and postoverwintering winter morphs (WM) over physiological age (degree-days, DD). In both morphs, reproductive rates were higher and lifespan was longer when flies were exposed to low protein (P:C 1:4) or carbohydrate-only diets (P:C 0:1) compared with high protein diets (P:C 1:1). WM had higher reproductive rates and longer generation times than SM on optimal 1:4 diet in all trialed temperatures, but at the lowest temperatures, SM had higher reproductive rates than WM in carbohydrate-only and high protein diets. This likely reflected delayed oogenesis and hindered reproduction after an overwintering period in WM receiving suboptimal diets. Oviposition for SM and WM receiving 1:4 diet commenced from 0 to 100 DD, and peaked between 400 and 500 DD, earlier than flies receiving 0:1 diet. These results suggest that dietary protein has a crucial role in early oogenesis, particularly for postoverwintering WM. The parameters developed here reflect the population dynamics of D. suzukii before and after the crop growing season, an essential time for population buildup, survival, and early and late host infestation.

Seasonal Reproductive Biology of Drosophila suzukii (Diptera: Drosophilidae) in Temperate Climates.

Drosophila suzukii (Matsumura; Diptera: Drosophilidae) is a key pest of sweet cherry and small fruits worldwide. The present studies were designed to describe the reproductive physiology in both sexes, through dissections of their reproductive organs. We extensively dissected female D. suzukii throughout the season from 2013 to 2016 and classified the reproductive status flies based on five recognizable ovarian maturation stages: 1) no ovaries; 2) unripe ovaries 3) ripening eggs in ovarioles; 4) mature eggs in ovarioles; and 5) mature eggs in the abdomen. Development was examined as a function of calendar days as well as degree-days (DD). Results obtained from winter collections revealed that females collected from November to March contained a lower percentage of mature eggs than females collected from April to September. These data suggest that environmental conditions during the dormant period induce reproductive diapause. Oogenesis likely increased with an increase in mean monthly temperatures and DD. The first overwintered females with mature eggs were dissected as early as 21 February 2014 in Trento (7 DD). Additionally, we found that a low proportion of males (less than 50%) had sperm in their testes between January and March, yet during the same period females already have sperm stored in their spermathecal. Ivy berries was an alternative but unfavorable non-crop host during the late dormant period, as evidenced by emergence of smaller adults when compared to individuals emerging from cherry fruits. This study showed that D. suzukii females have great potential for oviposition early in the season, posing a risk to early season maturing crop hosts.

Influence of Crop Management and Environmental Factors on Wolf Spider Assemblages (Araneae: Lycosidae) in an Australian Cotton Cropping System.

Wolf spiders (Lycosidae) are the most abundant ground-hunting spiders in the Australian cotton (Gossypium hirsutum L.) agroecosystems. These spiders have potential in controlling pest bollworms, Helicoverpa spp. (Lepidoptera: Noctuidae) in minimum-tilled fields. A study was carried out during a wet growing season (2011-2012) in Narrabri, New South Wales, Australia, to determine how different crop rotations and tillage affect wolf spider assemblages in cotton fields. Spider abundance and species richness did not differ significantly between simple plots (no winter crop) and complex plots (cotton-wheat Triticum aestivum L.-vetch Vicia benghalensis L. rotation). However, the wolf spider biodiversity, as expressed by the Shannon-Weaver and Simpson's indices, was significantly higher in complex plots. Higher biodiversity reflected a more even distribution of the most dominant species (Venatrix konei Berland, Hogna crispipes Koch, and Tasmanicosa leuckartii Thorell) and the presence of more rare species in complex plots. T. leuckartii was more abundant in complex plots and appears to be sensitive to farming disturbances, whereas V. konei and H. crispipes were similarly abundant in the two plot types, suggesting higher resilience or recolonizing abilities. The demographic structure of these three species varied through the season, but not between plot types. Environmental variables had a significant effect on spider assemblage, but effects of environment and plot treatment were overshadowed by the seasonal progression of cotton stages. Maintaining a high density and even distribution of wolf spiders that prey on Helicoverpa spp. should be considered as a conservation biological control element when implementing agronomic and pest management strategies.