Landscape-scale spatiotemporal dynamics of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) populations: implications for spatially-based pest management.

BACKGROUND: Brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), is an invasive and severe pest of specialty and row crops. A 2-year field study conducted in four Mid-Atlantic states in the USA characterized the spatial and temporal dynamics of BMSB populations and its association with landscape elements in commercial agriculture settings. In each state, two 1 km2 sites included typical landscape elements (i.e., tree fruit orchards, annual field and vegetable crops, woodlands, and human-made structures). Twenty-seven georeferenced pheromone traps were deployed per site and the number of BMSB adults and nymphs captured was counted throughout the growing season. RESULTS: Findings from spatial analysis by distance indices, along with time-series maps of BMSB distribution, showed that BMSB exhibited significant spatial aggregation, and that its distribution was spatially consistent between years. Analyses with geographic information systems (GIS) revealed that BMSB 'hot spots' occurred in different landscape elements throughout each season. Most patches (i.e., clusters of significantly higher trap captures) were found near woodlands early in the season, near tree fruit orchards in summer, and on the border of annual field crops in autumn. Buffer analysis with GIS indicated that more BMSB adults were captured closer to woodlands compared with other landscape elements. CONCLUSION: Understanding the spatial and temporal movement and distribution of BMSB is critical to predicting their potential impact and ultimately devising strategies to mitigate this risk to vulnerable crops. The results of this study can be used to design streamlined, spatially-based areawide management of BMSB in heterogeneous and complex agricultural landscapes. © 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.

Extended Sentinel Monitoring of Helicoverpa zea Resistance to Cry and Vip3Aa Toxins in Bt Sweet Corn: Assessing Changes in Phenotypic and Allele Frequencies of Resistance.

Transgenic corn and cotton that produce Cry and Vip3Aa toxins derived from Bacillus thuringiensis (Bt) are widely planted in the United States to control lepidopteran pests. The sustainability of these Bt crops is threatened because the corn earworm/bollworm, Helicoverpa zea (Boddie), is evolving a resistance to these toxins. Using Bt sweet corn as a sentinel plant to monitor the evolution of resistance, collaborators established 146 trials in twenty-five states and five Canadian provinces during 2020-2022. The study evaluated overall changes in the phenotypic frequency of resistance (the ratio of larval densities in Bt ears relative to densities in non-Bt ears) in H. zea populations and the range of resistance allele frequencies for Cry1Ab and Vip3Aa. The results revealed a widespread resistance to Cry1Ab, Cry2Ab2, and Cry1A.105 Cry toxins, with higher numbers of larvae surviving in Bt ears than in non-Bt ears at many trial locations. Depending on assumptions about the inheritance of resistance, allele frequencies for Cry1Ab ranged from 0.465 (dominant resistance) to 0.995 (recessive resistance). Although Vip3Aa provided high control efficacy against H. zea, the results show a notable increase in ear damage and a number of surviving older larvae, particularly at southern locations. Assuming recessive resistance, the estimated resistance allele frequencies for Vip3Aa ranged from 0.115 in the Gulf states to 0.032 at more northern locations. These findings indicate that better resistance management practices are urgently needed to sustain efficacy the of corn and cotton that produce Vip3Aa.

Revisiting fall armyworm population movement in the United States and Canada.

Introduction: Biophysical approaches validated against haplotype and trap catch patterns have modeled the migratory trajectory of fall armyworms at a semi-continental scale, from their natal origins in Texas or Florida through much of the United States east of the Rocky Mountains. However, unexplained variation in the validation analysis was present, and misalignments between the simulated movement patterns of fall armyworm populations and the haplotype ratios at several locations, especially in the northeastern US and Canada, have been reported. Methods: Using an expanded dataset extending into Canada, we assess the consistency of haplotype patterns that relate overwintered origins of fall armyworm populations to hypothesized dispersal trajectories in North America and compare the geographic distribution of these patterns with previous model projections. Results and discussion: We confirm the general accuracy of previous modeling efforts, except for late in the season where our data suggests a higher proportion of Texas populations invading the northeast, extending into eastern Canada. We delineate geographic limits to the range of both overwintering populations and show that substantial intermixing of the Texas and Florida migrants routinely occurs north of South Carolina. We discuss annual variation to these migratory trajectories and test the hypothesis that the Appalachian Mountains influence geographic patterns of haplotypes. We discuss how these results may limit gene flow between the Texas and Florida natal populations and limit the hereditary consequences of interbreeding between these populations.

Pest population dynamics are related to a continental overwintering gradient.

Overwintering success is an important determinant of arthropod populations that must be considered as climate change continues to influence the spatiotemporal population dynamics of agricultural pests. Using a long-term monitoring database and biologically relevant overwintering zones, we modeled the annual and seasonal population dynamics of a common pest, Helicoverpa zea (Boddie), based on three overwintering suitability zones throughout North America using four decades of soil temperatures: the southern range (able to persist through winter), transitional zone (uncertain overwintering survivorship), and northern limits (unable to survive winter). Our model indicates H. zea population dynamics are hierarchically structured with continental-level effects that are partitioned into three geographic zones. Seasonal populations were initially detected in the southern range, where they experienced multiple large population peaks. All three zones experienced a final peak between late July (southern range) and mid-August to mid-September (transitional zone and northern limits). The southern range expanded by 3% since 1981 and is projected to increase by twofold by 2099 but the areas of other zones are expected to decrease in the future. These changes suggest larger populations may persist at higher latitudes in the future due to reduced low-temperature lethal events during winter. Because H. zea is a highly migratory pest, predicting when populations accumulate in one region can inform synchronous or lagged population development in other regions. We show the value of combining long-term datasets, remotely sensed data, and laboratory findings to inform forecasting of insect pests.

CropPol: A dynamic, open and global database on crop pollination.

Seventy five percent of the world's food crops benefit from insect pollination. Hence, there has been increased interest in how global change drivers impact this critical ecosystem service. Because standardized data on crop pollination are rarely available, we are limited in our capacity to understand the variation in pollination benefits to crop yield, as well as to anticipate changes in this service, develop predictions, and inform management actions. Here, we present CropPol, a dynamic, open, and global database on crop pollination. It contains measurements recorded from 202 crop studies, covering 3,394 field observations, 2,552 yield measurements (i.e., berry mass, number of fruits, and fruit density [kg/ha], among others), and 47,752 insect records from 48 commercial crops distributed around the globe. CropPol comprises 32 of the 87 leading global crops and commodities that are pollinator dependent. Malus domestica is the most represented crop (32 studies), followed by Brassica napus (22 studies), Vaccinium corymbosum (13 studies), and Citrullus lanatus (12 studies). The most abundant pollinator guilds recorded are honey bees (34.22% counts), bumblebees (19.19%), flies other than Syrphidae and Bombyliidae (13.18%), other wild bees (13.13%), beetles (10.97%), Syrphidae (4.87%), and Bombyliidae (0.05%). Locations comprise 34 countries distributed among Europe (76 studies), North America (60), Latin America and the Caribbean (29), Asia (20), Oceania (10), and Africa (7). Sampling spans three decades and is concentrated on 2001-2005 (21 studies), 2006-2010 (40), 2011-2015 (88), and 2016-2020 (50). This is the most comprehensive open global data set on measurements of crop flower visitors, crop pollinators and pollination to date, and we encourage researchers to add more datasets to this database in the future. This data set is released for non-commercial use only. Credits should be given to this paper (i.e., proper citation), and the products generated with this database should be shared under the same license terms (CC BY-NC-SA).

Phenology, Development, and Parasitism of Allium Leafminer (Diptera: Agromyzidae), a Recent Invasive Species in the United States.

Allium leafminer, Phytomyza gymnostoma (Diptera: Agromyzidae), is an invasive species first recorded in the Western Hemisphere in 2015 and has expanded its range into northeastern and MidAtlantic states. Its host range encompasses Allium species grown for food and ornamentals, weedy species, species used for pollinator provisioning, and species of conservation concern. Using field and laboratory studies, we advanced methods for rearing, developed a phenology model for spring emergence, describe pupal development, and report on parasitism. Spring emergence was best detected by scouting wild alliums as opposed to emergence cages, and modeled using 350 degree-days above a lower threshold of 1.0°C. Spring adult flight occurred for about 5 wk. Larval development required 22 and 20 d at 17.5 and 25°C, respectively. Pupal development progressed along a color gradient, and an initial presence of fat cell clusters and an air bubble, followed by an exarate pupa. Pupal developed at 3-5% per day at 3°C and reached 25% per day at 21.5°C, but development was not successful at 30°C. Although parasitism rates were low, we documented two Chalcidoidea parasitoids, Halticoptera circulus (Walker) (Hymenoptera: Pteromalidae) and Chrysocharis oscinidis Ashmead (Hymenoptera: Pteromalidae). Together, these data provide baseline information to advance IPM for this invasive species both in crops and noncrop areas.

Parasitoids, Nematodes, and Protists in Populations of Striped Cucumber Beetle (Coleoptera: Chrysomelidae).

The striped cucumber beetle, Acalymma vittatum (Fabricius), is an important pest of cucurbit production in the eastern United States, where most commercial producers rely on insecticides to control this pest species. Biological control provides an alternative to insecticide use, but for A. vittatum, top-down control has not been well developed. In the northeastern United States, two parasitoid species, Celatoria setosa (Coquillett) (Diptera: Tachinidae) and Centistes diabroticae (Gahan) (Hymenoptera: Braconidae) have been reported from A. vittatum, but their distribution is poorly known. To determine whether these parasitoid species are attacking A. vittatum in Pennsylvania and the amount of mortality they provide, we characterized the parasitoid dynamics in two distinct efforts. First, we reared parasitoids from beetles captured at two research farms. Second, we focused on one of these farms and dissected beetles to quantify both parasitoid and parasite species attacking A. vittatum. Both efforts confirmed Cl. setosa and Cn. diabroticae, and parasitism rates varied widely between locations and among years (4-60%). Unexpectedly, our dissections revealed that a potentially undescribed nematode species (Howardula sp.) as the most common parasite in the community. We also discovered gregarine protists. Despite being smaller than females, males were more commonly attacked by parasitic species, but we detected no relationship between the size of beetles and abundance of parasitic species in A. vittatum. This work provides a baseline understanding of the parasitoid and parasite community attacking A. vittatum and advances opportunities for conservation biological control using these natural-enemy species.

The Influence of Marking Methods on Mobility, Survivorship, and Field Recovery of Halyomorpha halys (Hemiptera: Pentatomidae) Adults and Nymphs.

Halyomorpha halys (Stål), the brown marmorated stink bug, is an invasive and highly polyphagous insect that has caused serious economic injury to specialty and row crops in the United States and Europe. Here, we evaluated the effects of marking adult and nymphal H. halys with four different colors of fluorescent powder (Blaze Orange, Corona Pink, Horizon Blue, and Signal Green) on mobility and survivorship in laboratory bioassays. Adults and nymphs were marked using liquified fluorescent powder solutions and allowed to dry prior to bioassay. The presence of the marking solution had no significant effects on adult or nymphal mobility, adult survivorship, nymphal development, or adult flight capacity. We also evaluated the persistence of neon marker applied to the pronotum of H. halys adults and found this technique remained detectable for 2 wk under field conditions. Although both marking techniques are inexpensive, persist for ≥1 wk, and do not affect mortality, the neon marker method is more time-consuming, taking ~12 times longer to mark 50 adult H. halys compared with the liquified fluorescent powders. Thus, we would recommend using fluorescent powders for large-scale mark-release-recapture studies.

Temporal Variation in Genetic Composition of Migratory Helicoverpa Zea in Peripheral Populations.

Migrant populations of Helicoverpa zea (Boddie) captured during 2002, 2005, 2016, and 2018 from Landisville and Rock Springs in Pennsylvania, USA were genotyped using 85 single nucleotide polymorphism (SNP) markers. Samples (n = 702) genotyped were divided into 16 putative populations based on collection time and site. Fixation indices (F-statistics), analysis of molecular variance, and discriminant analysis of principal components were used to examine within and among population genetic variation. The observed and expected heterozygosity in putative populations ranged from 0.317-0.418 and 0.320-0.359, respectively. Broad range of FST (0.0-0.2742) and FIS (0.0-0.2330) values indicated different genotype frequencies between and within the populations, respectively. High genetic diversity within and low genetic differentiation between populations was found in 2002 and 2005. Interestingly, high genetic differentiation between populations from two collection sites observed in 2018 populations was not evident in within-site comparisons of putative populations collected on different dates during the season. The shift of H. zea population genetic makeup in 2018 may be influenced by multiple biotic and abiotic factors including tropical storms. Continued assessment of these peripheral populations of H. zea will be needed to assess the impacts of genetic changes on pest control and resistance management tactics.

Managing Allium Leafminer (Diptera: Agromyzidae): An Emerging Pest of Allium Crops in North America.

Allium leafminer, Phytomyza gymnostoma Loew, is the newest invasive pest of allium crops in North America. Larvae initially feed in the upper canopy before mining toward the base of the plant to pupate. Crop loss occurs when larvae destroy vascular tissue, facilitating infection by bacterial and fungal pathogens that cause rot. Contamination also occurs when larvae and pupae are present at harvest. In response to this invasion, efficacy of 14 insecticide active ingredients applied via foliar sprays, transplant treatments, and drip chemigation was evaluated for managing P. gymnostoma. Multiple field studies were conducted in onions, leeks, and scallions in Pennsylvania and New York, United States in 2018 and 2019. The highest and most consistent levels of P. gymnostoma control occurred using foliar applications of dinotefuran, cyantraniliprole and spinetoram (84-89% reduction in damage; 95% reduction in P. gymnostoma densities). Despite the success of dinotefuran and cyantraniliprole applied as foliar sprays, neither was effective in controlling P. gymnostoma when administered via drip chemigation. Other foliar-applied insecticides that significantly reduced densities of P. gymnostoma in one or two experiments included abamectin, acetamiprid, cyromazine, imidacloprid, lambda-cyhalothrin, methomyl, and spinosad. Active ingredients that never controlled P. gymnostoma included azadirachtin, kaolin clay, pyrethrin, and spirotetramat. Spinosad applied to bare-root and plug-tray transplants immediately before transplanting reduced P. gymnostoma damage in the field by >90%. Implications of using these insecticides and application strategies are discussed within the context of developing a sustainable IPM program.

Season-Long Monitoring of the Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) Throughout the United States Using Commercially Available Traps and Lures.

Reliable monitoring of the invasive Halyomorpha halys abundance, phenology and geographic distribution is critical for its management. Halyomorpha halys adult and nymphal captures on clear sticky traps and in black pyramid traps were compared in 18 states across the Great Lakes, Mid-Atlantic, Southeast, Pacific Northwest and Western regions of the United States. Traps were baited with commercial lures containing the H. halys pheromone and synergist, and deployed at field sites bordering agricultural or urban locations with H. halys host plants. Nymphal and adult captures in pyramid traps were greater than those on sticky traps, but captures were positively correlated between the two trap types within each region and during the early-, mid- and late season across all sites. Sites were further classified as having a low, moderate or high relative H. halys density and again showed positive correlations between captures for the two trap types for nymphs and adults. Among regions, the greatest adult captures were recorded in the Southeast and Mid-Atlantic on pyramid and sticky traps, respectively, with lowest captures recorded in the West. Nymphal captures, while lower than adult captures, were greatest in the Southeast and lowest in the West. Nymphal and adult captures were, generally, greatest during July-August and September-October, respectively. Trapping data were compared with available phenological models showing comparable population peaks at most locations. Results demonstrated that sticky traps offer a simpler alternative to pyramid traps, but both can be reliable tools to monitor H. halys in different geographical locations with varying population densities throughout the season.

Influence of host plant, geography and pheromone strain on genomic differentiation in sympatric populations of Ostrinia nubilalis.

Patterns of mating for the European corn borer (Ostrinia nubilalis) moth depend in part on variation in sex-pheromone blend. The ratio of (E)-11- and (Z)-11-tetradecenyl acetate (E11- and Z11-14:OAc) in the pheromone blend that females produce and males respond to differs between strains of O. nubilalis. Populations also vary in female oviposition preference for and larval performance on maize (C4) and nonmaize (C3) host plants. The relative contributions of sexual and ecological trait variation to the genetic structure of O. nubilalis remains unknown. Host-plant use (13 C/14 C ratios) and genetic differentiation were estimated among sympatric E and Z pheromone strain O. nubilalis males collected in sex-pheromone baited traps at 12 locations in Pennsylvania and New York between 2007 and 2010. Among genotypes at 65 single nucleotide polymorphism marker loci, variance at a position in the pheromone gland fatty acyl-reductase (pgfar) gene at the locus responsible for determining female pheromone ratio (Pher) explained 64% of the total genetic differentiation between males attracted to different pheromones (male response, Resp), providing evidence of sexual inter-selection at these unlinked loci. Principal coordinate, Bayesian clustering, and distance-based redundancy analysis (dbRDA) demonstrate that host plant history or geography does not significantly contribute to population variation or differentiation among males. In contrast, these analyses indicate that pheromone response and pgfar-defined strain contribute significantly to population genetic differentiation. This study suggests that behavioural divergence probably plays a larger role in driving genetic variation compared to host plant-defined ecological adaptation.

Documenting Potential Sunn Hemp (Crotalaria juncea L.) (Fabaceae) Pollinators in Florida.

Sunn hemp, Crotalaria juncea L., is a warm-season legume that can be planted in rotation to cash crops to add nitrogen and organic matter to the soils, for weed growth prevention, and to suppress nematode populations. Sunn hemp flowers also provide nectar and pollen for pollinators and enhance biological control by furnishing habitat for natural enemies. Experiments were conducted in Northern and North Central Florida to evaluate bee populations that visited flowers within mixed plots of sunn hemp and sorghum-sudangrass and plots of two sunn hemp germplasm lines. Collections of bees that visited 'AU Golden' and Tillage Sunn flowers indicated that Xylocopa virginica (L.) (Hymenoptera: Apidae), Xylocopa micans Lepeletier (Hymenoptera: Apidae), Megachile sculpturalis Smith (Hymenoptera: Megachilidae), Megachile mendica (Cresson) (Hymenoptera: Megachilidae), and Megachile georgica Cresson (Hymenoptera: Megachilidae) were present in large numbers in May through July and then again in October. Although Tillage Sunn seeds planted in March flowered in May, percent bloom and number of bee visits were low. Compared with short day sunn hemp cultivars, 'AU Golden' plants produced flowers early in the season to provide food and habitat for pollinators and have the potential to produce an abundant seed crop in Northern and North Central Florida.

Demonstration and Quantification of Restricted Mating Between Fall Armyworm Host Strains in Field Collections by SNP Comparisons.

Gene introgression between related pest populations is an important component in the assessment of how rapidly economically important traits, such as pesticide resistance, can spread within a region. An example of this is provided by the noctuid moth Spodoptera frugiperda (J.E. Smith), or fall armyworm, which is composed of two 'host strains' that differ in their host plant preferences. Resistance to a Bacillus thuringiensis toxin has been observed in some populations and there is concern about its spread throughout the Western Hemisphere. If this trait is easily transmitted between strains, it would expand the range of plants affected and make control efforts more difficult. A complicating factor is that the strains are morphologically indistinguishable and can only be identified by a small number of genetic markers. As a result, little is known about the frequency of interstrain hybridization in the wild. This study uses a novel strategy involving comparisons between two single-nucleotide polymorphisms (SNPs) to quantify the frequency of interstrain mating in field populations. The results demonstrate that hybridization between strains is 4- to 5-fold reduced compared to that within strains. In addition, it appears that directional interstrain mating biases observed in laboratory studies are probably not a major factor in determining the distribution of hybrid genotypes in field populations. The differential SNP technique is a significant improvement over current methods for identifying interstrain hybrids and should facilitate our understanding of fall armyworm strain and hybrid distributions in the field and the frequency of genetic exchanges between strains.

Phenology of brown marmorated stink bug described using female reproductive development.

Temperature-based degree-day models describe insect seasonality and to predict key phenological events. We expand on the use of a temperature-based process defining timing of reproduction through the incorporation of female reproductive physiology for the invasive pentatomid species Halyomorpha halys, the brown marmorated stink bug. A five-stage ranking system based on ovary development was able to distinguish between the reproductive statuses of field-collected females. Application of this ranking method described aspects of H. halys' seasonality, overwintering biology, and phenology across geographic locations. Female H. halys were collected in the US from NJ, WV, NC, OR, and two sites in PA in 2006-2008 (Allentown, PA only) and 2012-2014. Results identify that H. halys enters reproductive diapause in temperate locations in the fall and that a delay occurs in developmental maturity after diapause termination in the spring. Modification of the Snyder method to identify biofix determined 12.7-hr photoperiod as the best fit to define initiation of reproduction in the spring. Applying the biofix, we demonstrated significant differences between locations for the rate at which the overwintering generation transition into reproductive status and the factors contributing to this difference require further study. For example, after including abiotic variables influencing development such as temperature and photoperiod (critical diapause cue), reproduction occurred earlier in OR and for an extended period in NJ. This data describe a method to investigate insect seasonality by incorporating physiological development across multiple regions that can clarify phenology for insects with overlapping generations.

Corrigendum: Coupling Developmental Physiology, Photoperiod, and Temperature to Model Phenology and Dynamics of an Invasive Heteropteran, Halyomorpha halys.

[This corrects the article on p. 165 in vol. 7, PMID: 27242539.].

Correction: Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations.

[This corrects the article DOI: 10.1371/journal.pone.0171743.].

Landscape Factors Influencing Stink Bug Injury in Mid-Atlantic Tomato Fields.

Landscape structure and diversity influence insect species abundance. In agricultural systems, adjacent crop and non-crop habitats can influence pest species population dynamics and intensify economic damage. To investigate the influence of landscape factors on stink bug damage in agricultural systems, we assessed stink bug damage from 30 processing tomato fields in the mid-Atlantic United States and analyzed landscape structure and geographic location. We found that forest shape and size, and geographic location strongly influenced stink bug damage. Landscapes with larger forest edge in southern portions of the mid-Atlantic region experienced the greatest damage, perhaps owing to the introduction of the invasive brown marmorated stink bug. We conclude that landscape structure will likely influence damage rates in nearby agricultural fields.

Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations.

The fall armyworm, Spodoptera frugiperda (J. E. Smith)(Lepidoptera: Noctuidae), is an important agricultural pest of the Western Hemisphere noted for its broad host range, long distance flight capabilities, and a propensity to develop resistance to pesticides that includes a subset of those used in genetically modified corn varieties. These characteristics exacerbate the threat fall armyworm poses to agriculture, with the potential that a resistance trait arising in one geographical location could rapidly disseminate throughout the hemisphere. A region of particular concern is the Caribbean, where a line of islands that extends from Florida to Venezuela provides a potential migratory pathway between populations from North and South America that could allow for consistent and substantial genetic interactions. In this study, surveys of populations from Peru, Bolivia, Paraguay, and Trinidad & Tobago expand on previous work in South America that indicates a generally homogeneous population with respect to haplotype markers. This population differs from that found in most of the Lesser Antilles where a combination of genetic and meteorological observations is described that indicate fall armyworm migration from Puerto Rico to as far south as Barbados, but does not support significant incursion into Trinidad & Tobago and South America. Air transport projections demonstrate that the wind patterns in the Caribbean region are not conducive to consistent flight along the north-south orientation of the Lesser Antilles, supporting the conclusion that such migration is minor and sporadic, providing few opportunities for genetic exchanges. The implications of these findings on the dissemination of deleterious traits between the two Western Hemisphere continents are discussed.