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.
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.
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.
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•We compared parasitism of wild (field-laid) and sentinel (laboratory-laid) eggs.•Wild egg masses had higher parasitism, parasitoid abundance and species richness.•Anastatus reduvii ...was the most common parasitoid species overall.•Sentinel egg masses underestimate parasitoid communities and impact.•Wild egg masses should be used for estimating biological control impacts.
Native to eastern Asia, the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), has become a serious invasive pest in North America. Consequently, accurate assessment of parasitism rates under field conditions is critical for determining baseline parasitism rates of native egg parasitoids on BMSB, and for future evaluations of native or exotic parasitoid biological control release strategies and impacts. BMSB sentinel (laboratory-laid) egg masses have typically been used for this purpose, even though they could be providing misleading estimates of parasitoid activity. Accordingly, we compared the use of BMSB sentinel (laboratory-laid) and wild (naturally field-laid) egg masses in 2012 and 2013 to examine rates of parasitism and the parasitoid community composition of indigenous egg parasitoids in outdoor ornamental nurseries. Wild egg masses consistently had higher rates of parasitism than sentinel egg masses. In 2012, wild egg masses had a mean percent parasitism of 28.4% compared to 4.6% in sentinel egg masses, while in 2013 the difference between the two methods increased even further with a mean percent parasitism of 55.3% in wild egg masses compared to 0.8% in sentinel eggs. Furthermore, we found greater total numbers of parasitoids (889, 42) and greater species richness (seven, five), when using wild egg masses compared to sentinel egg masses, respectively. While sentinel egg masses provide a rapid and convenient way to assess the presence of natural enemies, our findings indicate that using sentinel egg masses could dramatically underestimate actual rates of parasitism and provide inaccurate estimates of parasitoid community composition. Future studies should address potential mechanisms underlying these patterns such as lack of certain host cues required by parasitoids in sentinel compared to wild egg masses.
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.
The emerald ash borer, Agrilus planipennis Fairmaire (EAB), is an invasive beetle that has caused widespread mortality of ash trees in North America. To date, four parasitoids have been introduced in ...North America for EAB biological control, including the egg parasitoid Oobius agrili Zhang & Huang (Hymenoptera: Encyrtidae). Monitoring EAB egg parasitism is challenging because female beetles oviposit in bark crevices and EAB eggs and O. agrili are small (<1 mm in diameter). Consequently, multiple methods have been developed to recover this parasitoid. Here we compared two methods, visual surveys and bark sifting, used to monitor establishment of O. agrili in Maryland, USA. From 2009 to 2015, a total of 56,176 O. agrili were released at 32 sites across the state. In 2016, we surveyed nine of the study sites for O. agrili establishment using both methods. We compared the amount of time spent searching for eggs separately in each method, and also analyzed the effects of years-post release, total number of parasitoids released, and median month of release, on percent parasitism of EAB eggs, and the percentage of trees per site with parasitized EAB eggs. We found that visually surveying ash trees for EAB eggs was more efficient than bark sifting; the percent parasitism observed using the two methods was similar, but visually surveying trees was more time-efficient. Both methods indicate that O. agrili can successfully establish populations in Maryland, and June may be the best month to release O. agrili in the state. Future research should investigate EAB phenology in the state to help optimize parasitoid release strategies.
Since the establishment of the brown marmorated stink bug,
Halyomorpha halys
(Stål) (Hemiptera: Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize ...the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of
H. halys
biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to
H. halys
egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically <10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking
H. halys
nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.
Specimens of an egg parasitoid wasp,
Telenomus cristatus
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
Halyomorpha halys
(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.
The emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), quickly established itself as an invasive species in North America after it was first detected near Detroit, Michigan, ...USA, in 2002. Just 1 yr later, emerald ash borer was introduced accidentally into Maryland, USA, on imported ash nursery stock. After quarantine and eradication efforts failed, a classical biological control program was initiated in Maryland in 2009 with the release of 2 larval parasitoids: Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius agrili Yang (Hymenoptera: Braconidae), and 1 egg parasitoid, Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae). Timing is critical to the success, efficiency, and cost-effectiveness of classical biological control programs where release of parasitoids must coincide temporally with that of susceptible stages of the host. In 2017, periodic field surveys at 2 sites in central Maryland were conducted to assess emerald ash borer phenology using green funnel traps to sample adults, and debarking infested ash trees to sample larval stages. Adult emerald ash borer first appeared in traps on 18 May 2017 (479 growing degree d base 10 GDD10), peaked on 15 Jun (823 GDD10), and were absent from 13 Jul (1,301 GDD10) through 12 Oct (2,598 GDD10) when surveys were terminated. Larval sampling in early Aug (1,698 GDD10) found all larval instars present, the most common being the second instar (46%), followed by the third instar (28%), fourth instar (20%), first instar (5%), and prepupal J-shaped larvae (J-larva) (0.5%). J-larvae are so called because after excavating a pupal chamber, the head is bent down 180 degrees to the rest of the body, resembling the shape of the letter J. Larval sampling in late Oct (2,710 GDD10) found J-larvae to be the dominant stage present (92.2%), followed by fourth instar (4.8%), third instar (2.4%), and second instar (0.6%). We found that emerald ash borer was univoltine, and that nearly 50% of emerald ash borer larvae had developed to stages susceptible to parasitism (third and fourth instar) by early Aug (1,698 GDD10). By late Oct (2,710 GDD10), 92% had developed beyond parasitoid susceptible stages (J-larvae). These findings suggest that egg parasitoid releases are best targeted from early May to late Jun at an approximate GDD10 range of 300 and 1,100 with larval parasitoid releases best targeted between 1,400 and 2,500 GDD10.
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.
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