Trissolcus japonicus (Ashmead) is an Asian egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stål). It has been under study in U.S. quarantine facilities since 2007 to evaluate its efficacy as a candidate classical biological control agent and its host specificity with regard to the pentatomid fauna native to the United States. A survey of resident egg parasitoids conducted in 2014 with sentinel egg masses of H. halys revealed that T. japonicus was already present in the wild in Beltsville, MD. Seven parasitized egg masses were recovered, of which six yielded live T. japonicus adults. All of these were in a wooded habitat, whereas egg masses placed in nearby soybean fields and an abandoned apple orchard showed no T. japonicus parasitism. How T. japonicus came to that site is unknown and presumed accidental.
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
Egg parasitoids of the exotic invasive brown marmorated stink bug, Halyomorpha halys (Stål), were investigated using lab-reared fresh (live) and frozen (killed) lab-reared sentinel egg masses deployed for 72h on foliage in three habitats—woods, orchard, and soybean field—in Maryland, USA, in summer 2014. Four native hymenopteran species, Telenomus podisi Ashmead (Scelionidae), Trissolcus euschisti (Ashmead) and Tr. brochymenae Ashmead (Scelionidae), and Anastatus reduvii (Howard) (Eupelmidae), developed and emerged from H. halys eggs. One exotic parasitoid, Trissolcus japonicus (Ashmead), emerged, providing the first known occurrence of this species in North America. Native parasitoids emerged from frozen eggs significantly more often than from fresh eggs (89.3% of egg masses and 98.1% of individual eggs), whereas the exotic Tr. japonicus did not show a similar difference, strongly suggesting adaptation to H. halys as a host by Tr. japonicus but not by the native species. Parasitoids were habitat-specific: all three Trissolcus species were significantly more likely to occur in the woods habitat, whereas Te. podisi was found exclusively in the soybean field. Further investigations are required to elucidate evolving host-parasitoid relationships, habitat specificity, and non-target effects of Tr. japonicus over the expanded range of H. halys in North America.
Biological invasions have far reaching effects on native plant and arthropod communities. This study evaluated the effect of natural enemies on eggs of the exotic invasive brown marmorated stink bug Halyomorpha halys (Stål) in experimental plots comprising species pairs of 16 ornamental trees and shrub genera from either Eurasia or North America and in wooded areas adjacent to the plots. Sentinel egg masses were placed on leaves of Acer, Cercis, Hydrangea, and Prunus in the plots and in seven genera of trees and shrubs in adjacent woods. Overall, rates of parasitism and predation in experimental plots were low, accounting for only 3.6 % and 4.5% of egg mortality, respectively. There were no significant differences in parasitism and predation rates between native or exotic plots or between plants of different genera. In 2015, predation was significantly higher in the experimental plots than in the wooded sites, but parasitism was significantly higher in the wooded sites. In the experimental plots, seven native and one exotic parasitoid species attacked sentinel egg masses. Six native parasitoid species attacked sentinel egg masses in the wooded sites. Parasitoids in the genus Trissolcus were more likely to attack egg masses in exotic plots than in native plots. There is no evidence that native natural enemies attacking eggs of the exotic BMSB were more prevalent in landscapes with native ornamental trees and shrubs than those with exotic trees and shrubs.
The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is attracted to its male-produced aggregation pheromone, a ~3.5:1 mixture of (3S,6S,7R,10S)- and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (SSRS and RSRS respectively), and also to the pheromone of its Asian sympatric species Plautia stali Scott (Hemiptera: Pentatomidae), methyl (2E,4E,6Z)-2,4,6-decatrienoate (MDT). A stereoisomeric mixture of (7R) 10,11-epoxy-1-bisabolen-3-ols (= mixed murgantiols) is used together in commercialized products with MDT because the latter is a synergist for H. halys attraction to mixed murgantiols. However, the optimal ratio for MDT combination with mixed murgantiols, and the sensitivity of bug captures to variation in ratio of the two pheromone components, have not been tested to date. Using black pyramid traps at two sites (in Maryland and West Virginia, United States), different ratios of mixed murgantiols to MDT were tested over two entire seasons. Also, captures using various ratios of the two active pheromone stereoisomers were undertaken in month-long trials with and without MDT. Results showed that H. halys adult and nymphal captures were relatively insensitive to the ratio of synthetic pheromone (mixed murgantiols) to MDT, as long as each was present in the trap. Captures of adults and nymphs were responsive to the lure loading of the SSRS isomer, but relatively insensitive to levels of the minor component, RSRS. The relative insensitivity of H. halys to these attractant ratios gives flexibility to development of more cost-efficient synthesis and trapping as well as other semiochemical-based management tactics.
Harlequin bug, Murgantia histrionica (Hahn) (Hemiptera: Pentatomidae), is a widespread pest that feeds on a variety of brassicaceous crops and other plants. To understand olfactory cues that mediate host-finding, and their possible utility in pest management, we deployed aggregation pheromone (mixed murgantiols = 10,11-epoxy-1-bisabolen-3-ols) and/or isothiocyanate (ITC) host plant volatiles with potted host plants and nonhost soybean, in field choice bioassays. Adults of both sexes were strongly attracted (10-31×) to collard host plants baited with pheromone lures, compared with unbaited collards, as were nymphs. Collard plants baited with lures containing allyl and/or benzyl-ITC showed a 1.3× and 1.9× increase in attractiveness, respectively, neither differing by life-stage nor sex; multiple lures showed additive attraction. Nonhost soybean, baited with pheromone lure, was 4.6-7.5× more attractive to adults than unbaited collard; conversely, baited collard was 124× more attractive than unbaited soybean. The stark difference in observed effect of pheromone lure between unpoisoned plants, and those poisoned with imidacloprid, indicated that attraction was underestimated by circa-daily counts of unpoisoned plants, presumably because if not poisoned, bugs rapidly abandoned the baited nonhost soybean plant. Results indicate that harlequin bugs can be misled to encounter and feed on nonhosts by their aggregation pheromone, but additional means may be needed to retain them. Attraction to hosts is increased both by the aggregation pheromone, and at least two host plant volatiles, allyl and benzyl-ITC. These results contribute to our knowledge of host finding in harlequin bug, and to possible trapping and trap cropping schemes for pest management.
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