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.

Telenomuscristatus Johnson (Hymenoptera, Scelionidae): new diagnostic data, distribution records and host associations.

Specimens of an egg parasitoid wasp, Telenomuscristatus Johnson (Platygastroidea, Scelionidae), were reared from stink bug egg masses collected in the wild, in Maryland, United States. The egg masses were identified morphologically as Halyomorphahalys (Stål), Banasa Stål and Euschistus Dallas (Hemiptera, Pentatomidae). Molecular tools were used to further identify the Euschistus egg masses as E.servus (Say) and E.tristigmus (Say). All of these are new host associations for Te.cristatus. We also provide data to contribute to future identification of Te.cristatus: images of the holotype specimen and COI sequences from two disparate localities.

Do adult Magicicada (Hemiptera: Cicadidae) feed? Historical perspectives and evidence from molecular gut content analysis.

The periodical cicadas in the genus Magicicada are remarkable for their unusual life histories and dramatic synchronized emergences every 13 or 17 years. While aspects of their evolution, mating behaviors, and general biology have been well-characterized, there is surprising uncertainty surrounding the feeding habits of the short-lived adult stage. Despite a tentative scientific consensus to the contrary, the perception that adult Magicicada do not feed has persisted among the general public, and recent studies are lacking. We directly investigated the feeding behavior of Magicicada spp. through high-throughput sequencing (HTS)-based dietary analysis of nymphs, freshly molted (teneral) adults, and fully sclerotized adults collected from orchard and wooded habitats during the 2021 emergence of Brood X. Identifiable plant DNA (trnF, ITS amplicons) was successfully recovered from nymphs and adults. No plant DNA was recovered from teneral adults, suggesting that all DNA recovered from sclerotized adults was ingested during the post-teneral adult stage. Both nymphs and adults were found to have ingested a range of woody and herbaceous plants across 17 genera and 14 families. Significantly more plant genera per individual were recovered from adults than from nymphs, likely reflecting the greater mobility of the adult stage. We hypothesize that the demonstrated ingestion of plant sap by Magicicada adults is driven by a need to replace lost water and support specialized bacteriome-dwelling endosymbionts that cicadas depend upon for growth and development, which constitutes true feeding behavior.

Protective neighboring effect from ash trees treated with systemic insecticide against emerald ash borer.

BACKGROUND: The emerald ash borer (EAB) (Agrilus planipennis Fairmaire) (Coleoptera: Buprestidae) is now the most destructive invasive species in North America. While biocontrol using parasitoids shows promising results in natural forests, strategies are needed to protect high-value trees against invasive EAB populations. Emamectin benzoate is a commonly used systemic insecticide for the protection of valuable trees. Methods that optimize its use allow for reduced quantities of insecticide to be released in the environment and save time and money in efforts to protect ash trees from EAB. We hypothesize that a treated tree can also offer a protective neighboring effect to nearby untreated ash trees, allowing for an optimized spatial planning of insecticide applications. RESULTS: We sampled 896 untreated ash trees, in the vicinity of treated trees, in Maryland and Washington DC. We recorded signs of EAB infestation (canopy condition, exit holes, wood pecks, epicormic growth, and bark splits). Two subsequent yearly samplings were made of 198 and 216 trees, respectively. We also present a novel proximity index for this particular application. Results show consistent decrease in EAB infestation signs in untreated trees as proximity to treated trees increases. CONCLUSION: Results support that a neighboring effect occurs. However, proximity to treated trees must be high for a tree to be safely left untreated. This proximity seems rare in forests, but can happen in urban/planted landscapes. Future studies should test and validate these findings, and could lead to a more precise recommended safe index tailored across multiple ash species and geographic regions.

Influence of Landscape Factors and Abiotic Conditions on Dispersal Behavior and Overwintering Site Selection by Halyomorpha halys (Hemiptera: Pentatomidae).

Since the initial detection of the invasive Halyomorpha halys (Stål) in the United States in the late 1990s, this insect has emerged as a severe agricultural and nuisance pest. Nuisance problems are due to adult dispersal to overwintering sites in the fall at which time they alight onto and eventually settle within human-made structures in addition to natural harborage. This study examined how three factors, elevation, light, and moisture affected overwintering site selection by H. halys in the mid-Atlantic. Observational counts performed along elevational transects revealed elevation was significant predictor of H. halys abundance during both years of the study in 2014 and 2015 with more adults observed at higher elevations. Choice tests examining effects of moisture and light on settling behavior demonstrated H. halys settled within overwintering shelter boxes in significantly greater numbers when shelters were dry compared with those having moist conditions, and in darkened shelters compared with those augmented with LED lights. Our findings indicate that H. halys use cues at both landscape and very localized levels when seeking and selecting overwintering sites.

Enhanced Response of Halyomorpha halys (Hemiptera: Pentatomidae) to Its Aggregation Pheromone with Ethyl Decatrienoate.

The invasive stink bug species, Halyomorpha halys (Stål) (Hemiptera; Pentatomidae), severely damages multiple agricultural commodities, resulting in the disruption of established IPM programs. Several semiochemicals have been identified to attract H. halys to traps and monitor their presence, abundance, and seasonal activity. In particular, the two-component aggregation pheromone of H. halys, (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (PHER), in combination with the pheromone synergist, methyl (2E,4E,6Z)-decatrienoate (MDT), were found to be attractive. Here, we report that an analogous trienoate, ethyl (2E,4E,6Z)-decatrienoate (EDT), enhances H. halys captures when combined with PHER. In trials conducted in Eastern and Western regions of the United States, we observed that when traps were baited with the H. halys PHER + EDT, captures were significantly greater than when traps were baited with PHER alone. Traps baited with EDT alone were not attractive. Thus, the addition of EDT to lures for attracting H. halys to traps may further improve monitoring efficiency and management strategies for this invasive species.

Climate variation alters the synchrony of host-parasitoid interactions.

Observed changes in mean temperature and increased frequency of extreme climate events have already impacted the distributions and phenologies of various organisms, including insects. Although some research has examined how parasitoids will respond to colder temperatures or experimental warming, we know relatively little about how increased variation in temperature and humidity could affect interactions between parasitoids and their hosts. Using a study system consisting of emerald ash borer (EAB), Agrilus planipennis, and its egg parasitoid Oobius agrili, we conducted environmentally controlled laboratory experiments to investigate how increased seasonal climate variation affected the synchrony of host-parasitoid interactions. We hypothesized that increased climate variation would lead to decreases in host and parasitoid survival, host fecundity, and percent parasitism (independent of host density), while also influencing percent diapause in parasitoids. EAB was reared in environmental chambers under four climate variation treatments (standard deviations in temperature of 1.24, 3.00, 3.60, and 4.79°C), while O. agrili experiments were conducted in the same environmental chambers using a 4 × 3 design (four climate variation treatments × 3 EAB egg densities). We found that EAB fecundity was negatively associated with temperature variation and that temperature variation altered the temporal egg laying distribution of EAB. Additionally, even moderate increases in temperature variation affected parasitoid emergence times, while decreasing percent parasitism and survival. Furthermore, percent diapause in parasitoids was positively associated with humidity variation. Our findings indicate that relatively small changes in the frequency and severity of extreme climate events have the potential to phenologically isolate emerging parasitoids from host eggs, which in the absence of alternative hosts could lead to localized extinctions. More broadly, these results indicate how climate change could affect various life history parameters in insects, and have implications for consumer-resource stability and biological control.

Field surveys of egg mortality and indigenous egg parasitoids of the brown marmorated stink bug, Halyomorpha halys, in ornamental nurseries in the mid-Atlantic region of the USA.

The brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive species native to regions of China, Japan, Korea, and Taiwan. In its native and introduced range, H. halys is considered a pest of tree fruits, vegetables, legumes, and ornamental trees. The highly polyphagous nature of this insect as well as its vast dispersal capabilities, require an integrated approach to management. Here we focus on the potential impact of indigenous natural enemies on H. halys in woody ornamental nurseries in Maryland, USA. We sampled naturally field laid H. halys egg masses for mortality and parasitism rates in 2012 and 2013. Overall, egg mortality averaged 54% for both years, and increased within season and between years. The largest source of mortality was from egg parasitoids with mean parasitism rates of 30.73 and 39.63% in 2012 and 2013, respectively. Mortality from predation was much lower and averaged 4.61% by chewing and 2.53% by sucking predators. We found seven species of Hymenopteran egg parasitoids attacking H. halys eggs, with Anastatus reduvii being the dominant species comprising 61.17 and 79.12% of all parasitoids in 2012 and 2013, respectively. The observed increase in parasitism over time and female biased sex ratio of parasitoids suggests that native parasitoids may be responding to the novel host, H. halys. Consequently, the use of these native eupelmid egg parasitoids in augmentative or conservation biological control may be a viable H. halys management strategy in ornamental nurseries.

Invasive stink bug favors naïve plants: Testing the role of plant geographic origin in diverse, managed environments.

With the introduction and establishment of exotic species, most ecosystems now contain both native and exotic plants and herbivores. Recent research identifies several factors that govern how specialist herbivores switch host plants upon introduction. Predicting the feeding ecology and impacts of introduced generalist species, however, remains difficult. Here, we examine how plant geographic origin, an indicator of shared co-evolutionary history, influences patterns of host use by a generalist, invasive herbivore, while accounting for variation in plant availability. The brown marmorated stink bug, Halyomorpha halys, is a highly polyphagous Asian herbivore and an economically important invasive pest in North America and Europe. In visual surveys of 220 plant taxa in commercial nurseries in Maryland, USA, H. halys was more abundant on non-Asian plants and selected these over Asian plants. The relationship between the relative use of plants and their availability was strongly positive but depended also on plant origin at two of our three sites, where the higher relative use of non-Asian plants was greatest for highly abundant taxa. These results highlight the importance of considering both plant origin and relative abundance in understanding the selection of host plants by invasive generalist herbivores in diverse, natural and urban forests.

Host Plant Use by the Invasive Halyomorpha halys (Stål) on Woody Ornamental Trees and Shrubs.

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an invasive plant-feeding insect native to eastern Asia. This herbivore is highly polyphagous, feeding on and damaging diverse plants, including field crops, vegetables, tree fruits, and ornamentals. Woody ornamental plants provide early- and late-season resources for adults emerging from and returning to overwintering sites, as well as feeding and breeding sites for H. halys throughout the growing season. In this study, we quantify the use of diverse plants by H. halys in two commercial nurseries in Maryland, recording data on the abundance of egg masses, early and late instar nymphs, and adults over a three-year study period. Our specific goals were to provide a quantitative comparison of the use of diverse plant species and cultivated varieties, identify non-hosts that could be used to create landscapes refractory to H. halys, and determine whether the use of plants varied across life stages of H. halys or the taxonomic status of plants. We found broad use of diverse plants in this study, identifying 88 host plants used by all life stages of H. halys. We also highlight the 43 plant taxa that did not support any life stage of H. halys and are thus classified as non-hosts. Interestingly, some of these plants were congeners of highly-used plants, underscoring high intrageneric and intraspecific variation in the use of plants by this polyphagous herbivore. We discuss how the selective planting of non-hosts, especially gymnosperms, may aid in reducing the agricultural and nuisance pest status of this invasive insect.

Edge Effects Influence the Abundance of the Invasive Halyomorpha halys (Hemiptera: Pentatomidae) in Woody Plant Nurseries.

The invasive brown marmorated stink bug, Halyomorpha halys (Stål), has caused severe economic losses in the United States and is also a major nuisance pest invading homes. In diverse woody plant nurseries, favored host plants may be attacked at different times of the season and in different locations in the field. Knowledge of factors influencing H. halys abundance and simple methods to predict where H. halys are found and cause damage are needed to develop effective management strategies. In this study, we examined H. halys abundance on plants in tree nurseries as a function of distance from field edges (edge and core samples) and documented the abundance in tree nurseries adjoining different habitat types (corn, soybean, residential areas, and production sod). We conducted timed counts for H. halys on 2,016 individual trees belonging to 146 unique woody plant cultivars at two commercial tree nurseries in Maryland. Across three years of sampling, we found that H. halys nymphs and adults were more abundant at field edges (0-5 m from edges) than in the core of fields (15-20 m from edges). Proximity of soybean fields was associated with high nymph and adult abundance. Results indicate that monitoring efforts and intervention tactics for this invasive pest could be restricted to field edges, especially those close to soybean fields. We show clearly that spatial factors, especially distance from edge, strongly influence H. halys abundance in nurseries. This information may greatly simplify the development of any future management strategies.

Attraction of the Invasive Halyomorpha halys (Hemiptera: Pentatomidae) to Traps Baited with Semiochemical Stimuli Across the United States.

A recent identification of the two-component aggregation pheromone of the invasive stink bug species, Halyomorpha halys (Stål), in association with a synergist, has greatly improved the ability to accurately monitor the seasonal abundance and distribution of this destructive pest. We evaluated the attraction of H. halys to black pyramid traps baited with lures containing the pheromone alone, the synergist methyl (2E,4E,6Z)-decatrienoate (MDT) alone, and the two lures in combination. Traps were deployed around areas of agricultural production including fruit orchards, vegetables, ornamentals, or row crops in Delaware, Maryland, North Carolina, New Jersey, New York, Ohio, Oregon, Pennsylvania, Virginia, and West Virginia from mid-April to mid-October, 2012 and 2013. We confirmed that H. halys adults and nymphs are attracted to the aggregation pheromone season long, but that attraction is significantly increased with the addition of the synergist MDT. H. halys adults were detected in April with peak captures of overwintering adults in mid- to late May. The largest adult captures were late in the summer, typically in early September. Nymphal captures began in late May and continued season long. Total captures declined rapidly in autumn and ceased by mid-October. Captures were greatest at locations in the Eastern Inland region, followed by those in the Eastern Coastal Plain and Pacific Northwest. Importantly, regardless of location in the United States, all mobile life stages of H. halys consistently responded to the combination of H. halys aggregation pheromone and the synergist throughout the entire season, suggesting that these stimuli will be useful tools to monitor for H. halys in managed systems.

Quantifying the impact of woodpecker predation on population dynamics of the emerald ash borer (Agrilus planipennis).

The emerald ash borer (EAB), Agrilus planipennis, is an invasive beetle that has killed millions of ash trees (Fraxinus spp.) since it was accidentally introduced to North America in the 1990s. Understanding how predators such as woodpeckers (Picidae) affect the population dynamics of EAB should enable us to more effectively manage the spread of this beetle, and toward this end we combined two experimental approaches to elucidate the relative importance of woodpecker predation on EAB populations. First, we examined wild populations of EAB in ash trees in New York, with each tree having a section screened to exclude woodpeckers. Second, we established experimental cohorts of EAB in ash trees in Maryland, and the cohorts on half of these trees were caged to exclude woodpeckers. The following spring these trees were debarked and the fates of the EAB larvae were determined. We found that trees from which woodpeckers were excluded consistently had significantly lower levels of predation, and that woodpecker predation comprised a greater source of mortality at sites with a more established wild infestation of EAB. Additionally, there was a considerable difference between New York and Maryland in the effect that woodpecker predation had on EAB population growth, suggesting that predation alone may not be a substantial factor in controlling EAB. In our experimental cohorts we also observed that trees from which woodpeckers were excluded had a significantly higher level of parasitism. The lower level of parasitism on EAB larvae found when exposed to woodpeckers has implications for EAB biological control, suggesting that it might be prudent to exclude woodpeckers from trees when attempting to establish parasitoid populations. Future studies may include utilizing EAB larval cohorts with a range of densities to explore the functional response of woodpeckers.

Ecology of herbivorous arthropods in urban landscapes.

Urbanization affects communities of herbivorous arthropods and provides opportunities for dramatic changes in their abundance and richness. Underlying these changes are creation of impervious surfaces; variation in the density, diversity, and complexity of vegetation; and maintenance practices including pulsed inputs of fertilizers, water, and pesticides. A rich body of knowledge provides theoretical underpinnings for predicting and understanding impacts of urbanization on arthropods. However, relatively few studies have elucidated mechanisms that explain patterns of insect and mite abundance and diversity across urbanization gradients. Published accounts suggest that responses to urbanization are often taxon specific, highly variable, and linked to properties of urbanization that weaken top-down and/or bottom-up processes, thereby destabilizing populations of herbivores and their natural enemies. In addition to revealing patterns in diversity and abundance of herbivores across urbanization gradients, a primary objective of this review is to examine mechanisms underlying these patterns and to identify potential hypotheses for future testing.

Spatial and temporal variation in natural enemy assemblages on Maryland native plant species.

Habitat manipulation is a branch of conservation biological control in which vegetation complexity and diversity are increased in managed landscapes to provide food and other resources for arthropod natural enemies. This is often achieved by maintaining noncrop plant material such as flowering strips and beetle banks that provide natural enemies with nectar and pollen, alternative prey, shelter from disturbance, and overwintering sites. In most cases, plant material used in habitat manipulation programs is not native to the area in which it is planted. Using native plant species in conservation biological control could serve a dual function of suppressing pest arthropod outbreaks and promoting other valuable ecosystem services associated with native plant communities. We evaluated 10 plant species native to Maryland for their attractiveness to foliar and ground-dwelling natural enemies. Plants that showed particular promise were Monarda punctata, Pycnanthemum tenuifolium, and Eupatorium hyssopifolium, which generally harbored the greatest abundance of foliar predators and parasitoids, although abundance varied over time. Among ground-dwelling natural enemies, total predator and parasitoid abundance differed between plant species, but carabid and spider abundance did not. Matching certain plant species and their allied natural enemies with specific pest complexes may be enhanced by identifying the composition of natural enemy assemblages at different times of year and in both foliar and ground habitat strata.

Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes?

This study examined the influence of habitat structural complexity on the collective effects of top-down and bottom-up forces on herbivore abundance in urban landscapes. The persistence and varying complexity of urban landscapes set them apart from ephemeral agroecosystems and natural habitats where the majority of studies have been conducted. Using surveys and manipulative experiments. We explicitly tested the effect of natural enemies (enemies hypothesis), host plant quality, and herbivore movement on the abundance of the specialist insect herbivore, Stephanitis pyrioides, in landscapes of varying structural complexity. This herbivore was extremely abundant in simple landscapes and rare in complex ones. Natural enemies were the major force influencing abundance of S. pyrioides across habitat types. Generalist predators, particularly the spider Anyphaena celer, were more abundant in complex landscapes. Predator abundance was related to greater abundance of alternative prey in those landscapes. Stephanitis pyrioides survival was lower in complex habitats when exposed to endemic natural enemy populations. Laboratory feeding trials confirmed the more abundant predators consumed S. pyrioides. Host plant quality was not a strong force influencing patterns of S. pyrioides abundance. When predators were excluded, adult S. pyrioides survival was greater on azaleas grown in complex habitats, in opposition to the observed pattern of abundance. Similarly, complexity did not affect S. pyrioides immigration and emigration rates. The complexity of urban landscapes affects the strength of top-down forces on herbivorous insect populations by influencing alternative prey and generalist predator abundance. It is possible that habitats can be manipulated to promote the suppressive effects of generalist predators.

Beat sampling accuracy in estimating spruce spider mite (Acari: Tetranychidae) populations and injury on juniper.

The use of a standardized beat sampling method for estimating spruce spider mite, Oligonychus ununguis (Jacobi) (Acari: Tetranychidae), densities on a widely used evergreen ornamental plant species, Juniperus chinensis variety 'Sargentii' A. Henry (Cupressaceae), was examined. There was a significant positive relationship between total spruce spider mite densities and spider mite densities from beat sampling on juniper. The slope and intercept of the relationship may be used by pest managers to predict total spider mite densities on plants from beat sample counts. Beat sampling dramatically underestimates the total number of spider mites on a foliage sample. The relationships between spruce spider mite feeding injury and spider mite density estimates from beat sampling juniper foliage and total spider mite counts on foliage were also examined. There was a significant positive relationship between spruce spider mite density as estimated from beat sampling and injury to the plants. There was a similar positive relationship between the total number of spruce spider mites and injury to the plants, suggesting that a pest manager could use beat sampling counts to estimate plant injury and related thresholds. These findings have important implications to decision-making for spruce spider mite control, especially as it relates to threshold levels and determining rates of predator releases. Further assessment of the effectiveness of beat and other sampling methods across multiple spider mite- host plant associations needs to be examined to enable pest managers to select sampling plans that are feasible and reliable.

Evaluation of predatory mite (Acari: Phytoseiidae) releases to suppress spruce spider mites, Oligonychus ununguis (Acari: Tetranychidae), on juniper.

A laboratory trial evaluated four phytoseiid species for their potential as biological control agents of spruce spider mite, Oligonychus ununguis (Jacobi) (Acari: Tetranychidae). An augmentative biological control approach, using the predatory mites Neoseiulus fallacis Garman and Galendromus occidentalis Nesbitt (Acari: Phytoseiidae), was evaluated for reducing pest mite densities and injury, and economic costs on Juniperus chinensis 'Sargentii' A. Henry (Cupressaceae) in an outdoor nursery. Sequential releases of predator species, individually and in combination, were tested and compared with two commonly used miticides, a low-toxicity miticide, horticultural oil, and a conventional miticide, hexythiazox. Timing of treatments was based on grower-determined need, and predator release rates were based on guidelines in literature received from producers of beneficial organisms. Predator releases were more expensive and provided less effective suppression of spruce spider mites, resulting in greater spider mite injury to plants, compared with conventional pesticides. However, spider mite damage to plants did not differ in an economically meaningful way between treatments. Unsatisfactory levels of control seem related to under estimations of actual spider mite abundance based on grower perceptions and the beat sampling technique used to estimate predator release rates. These data suggest that when initial populations of spruce spider mite are high, it is unlikely that sequential releases of predator species, individually or in combination, will suppress spider mite populations. In this trial, augmentative biological control control was 2.5-7 times more expensive than chemical controls.