Nik G. Wiman

Biology, Ecology, and Management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae)

Brown marmorated stink bug, Halyomorpha halys Stal, is an invasive, herbivorous insect species that was accidentally introduced to the United States from Asia. First discovered in Allentown, PA, in 1996, H. halys has now been reported from at least 40 states in the United States. Additional invasions have been detected in Canada, Switzerland, France, Germany, Italy, and Lichtenstein, suggesting this invasive species could emerge as a cosmopolitan pest species. In its native range, H. halys is classified as an outbreak pest; however, in North America, H. halys has become a major agricultural pest across a wide range of commodities. H. halys is a generalist herbivore, capable of consuming >100 different species of host plants, often resulting in substantial economic damage; its feeding damage resulted in US

Temperature-Related Development and Population Parameters for Drosophila suzukii (Diptera: Drosophilidae) on Cherry and Blueberry

37 million of losses in apple in 2010, but this stink bug species also attacks other fruit, vegetable, field crop, and ornamental plant species. H. halys has disrupted integrated pest management programs for multiple cropping systems. Pesticide applications, including broad-spectrum insecticides, have increased in response to H. halys infestations, potentially negatively influencing populations of beneficial arthropods and increasing secondary pest outbreaks. H. halys is also challenging because it affects homeowners as a nuisance pest; the bug tends to overwinter in homes and outbuildings. Although more research is required to better understand the ecology and biology of H. halys , we present its life history, host plant damage, and the management options available for this invasive pest species.

Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation

ABSTRACT Temperature-related studies were conducted on Drosophila suzukii Matsumura (Diptera: Drosophilidae: Drosophilini). From 10–28°C, temperature had a significant impact on blueberries, Vaccinium corymbosum L. (Ericales: Ericaceae), and cherries, Prunus avium (L.) L. 1755 (Rosales: Rosaceae), important commercial hosts of D. suzukii. Temperature had a significant influence on D. suzukii developmental period, survival, and fecundity, with decreasing developmental periods as temperatures increased to 28°C. At 30°C, the highest temperature tested, development periods increased, indicating that above this temperature the developmental extremes for the species were approached. D. suzukii reared on blueberries had lower fecundity than reared on cherries at all temperatures where reproduction occurred. The highest net reproductive rate (Ro) and intrinsic rate of population increase (r m) were recorded on cherries at 22°C and was 195.1 and 0.22, respectively. Estimations using linear and nonlinear fit for the minimum, optimal, and maximum temperatures where development can take place were respectively, 7.2, 28.1, and 42.1°C. The rm values were minimal, optimal, and maximal at 13.4, 21.0, and 29.3°C, respectively. Our laboratory cultures of D. suzukii displayed high rates of infection for Wolbachia spp. (Rickettsiales: Rickettsiaceae), and this infection may have impacted fecundity found in this study. A temperature-dependent matrix population estimation model using fecundity and survival data were run to determine whether these data could predict D. suzukii pressure based on environmental conditions. The model was applied to compare the 2011 and 2012 crop seasons in an important cherry production region. Population estimates using the model explained different risk levels during the key cherry harvest period between these seasons.

Humidity affects populations of Drosophila suzukii (Diptera: Drosophilidae) in blueberry

Temperature-dependent fecundity and survival data was integrated into a matrix population model to describe relative Drosophila suzukii Matsumura (Diptera: Drosophilidae) population increase and age structure based on environmental conditions. This novel modification of the classic Leslie matrix population model is presented as a way to examine how insect populations interact with the environment, and has application as a predictor of population density. For D. suzukii, we examined model implications for pest pressure on crops. As case studies, we examined model predictions in three small fruit production regions in the United States (US) and one in Italy. These production regions have distinctly different climates. In general, patterns of adult D. suzukii trap activity broadly mimicked seasonal population levels predicted by the model using only temperature data. Age structure of estimated populations suggest that trap and fruit infestation data are of limited value and are insufficient for model validation. Thus, we suggest alternative experiments for validation. The model is advantageous in that it provides stage-specific population estimation, which can potentially guide management strategies and provide unique opportunities to simulate stage-specific management effects such as insecticide applications or the effect of biological control on a specific life-stage. The two factors that drive initiation of the model are suitable temperatures (biofix) and availability of a suitable host medium (fruit). Although there are many factors affecting population dynamics of D. suzukii in the field, temperature-dependent survival and reproduction are believed to be the main drivers for D. suzukii populations.

Attraction of the invasive halyomorpha halys (Hemiptera: Pentatomidae) to traps baited with semiochemical stimuli across the United States

Temperature and humidity affect insect physiology, survival, fecundity, reproductive status and behaviour. Complementing previous work investigating the effects of temperature on adult survival and fecundity of the invasive frugivorous pest, Drosophila suzukii (Matsumura), this study was conducted to determine the effect of humidity on D. suzukii larval development, adult survival, fecundity and reproductive status using blueberry as a host substrate. The five constant humidity levels in laboratory bioassays were 20, 33, 71, 82 and 94% RH at 20.6 ± 0.2°C. As RH increased, fecundity and longevity increased. At the higher humidity levels, RH had limited impact on mean generation times (T), larval development and eclosion times. The highest net reproductive rate (Ro = 68) and highest intrinsic rate of population increase (rm = 0.17) were both recorded at 94% RH. The reproductive status of females, as indicated by the number of mature oocytes per female, was significantly greater at 82 and 94% RH, compared to 71% RH. In addition to the laboratory procedures, we correlated field trap captures over an 81‐day summer period to relative humidity (RH) levels in close proximity to those traps. In the field, low ambient humidity levels resulted in decreased trap captures. A humidity‐dependent population model predicted lower densities of D. suzukii relative to populations at higher humidity. This study supports the hypothesis that cultural practices that minimize lower humidity levels in crops can contribute to the management of D. suzukii. Such methods may include open pruning, drip irrigation and field floor management.

Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

ABSTRACT 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.

Characterizing Damage of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) in Blueberries

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.

Global invasion network of the brown marmorated stink bug, Halyomorpha halys

ABSTRACT Brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a severe economic pest of growing importance in the United States, Canada, and Europe. While feeding damage from H. halys has been characterized in tree fruit, vegetables, and agronomic crops, less is known about the impacts of stink bugs on small fruits such as blueberries. In this study, we examined H. halys feeding on two representative early and late ripening blueberry cultivars in Oregon and New Jersey. This research examined how different densities of H. halys confined on blueberry clusters for week-long periods affected fruit quality at harvest. After fruit were ripe, we stained and quantified the number of salivary sheaths on berries as an indication of feeding pressure. Feeding by H. halys damaged the fruits by causing increased levels of external discoloration, and internal damage in the form of tissue necrosis. Exposure of berries to H. halys was also associated with decreasing berry weights and lower soluble solids in fruits. However, the different cultivars did not respond consistently to feeding pressure from H. halys. Weekly variability in feeding pressure of two of the cultivars as quantified by the number of stylet sheaths per berry was largely accounted for by environmental variables. We conclude that H. halys does have potential to severely damage blueberries and may become an important economic pest. Characterization of damage is important because correct identification of insect damage is key for successful management.

Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon

Human mediated transportation into novel habitats is a prerequisite for the establishment of non-native species that become invasive, so knowledge of common sources may allow prevention. The brown marmorated stink bug (BMSB, Halyomorpha halys) is an East Asian species now established across North America and Europe, that in the Eastern United States of America (US) and Italy is causing significant economic losses to agriculture. After US populations were shown to originate from Northern China, others have tried to source BMSB populations now in Canada, Switzerland, Italy, France, Greece, and Hungary. Due to selection of different molecular markers, however, integrating all the datasets to obtain a broader picture of BMSB’s expansion has been difficult. To address this limitation we focused on a single locus, the barcode region in the cytochrome oxidase I mitochondrial gene, and analyzed representative BMSB samples from across its current global range using an Approximate Bayesian Computation approach. We found that China is the likely source of most non-native populations, with at least four separate introductions in North America and three in Europe. Additionally, we found evidence of one bridgehead event: a likely Eastern US source for the central Italy populations that interestingly share enhanced pest status.

Phenology of brown marmorated stink bug described using female reproductive development

Trissolcus japonicus is an egg parasitoid of Halyomorpha halys, brown marmorated stink bug, a severe agricultural pest in the USA. T. japonicus is being evaluated in quarantine as a classical biological control agent to manage H. halys populations in the USA. To determine T. japonicus’ potential for successful management of the pest, we performed a series of no-choice and paired-host-range tests, evaluating parasitism and host recognition in ten nontarget insects. In laboratory no-choice tests, T. japonicus successfully parasitized egg masses of seven Pentatomidae native to Oregon in addition to H. halys. Mean parasitism proportions of egg masses were greater than 40% in two species, B. dimidiata and H. abbreviatus, and were statistically similar to parasitism of H. halys. However, paired-host tests identified higher proportions of parasitized H. halys egg masses compared to four other pentatomids. T. japonicus was equally attracted to volatiles produced by H. halys and other pentatomids but demonstrated significantly longer arrestment response time on surfaces with H. halys contact kairomones. Although host acceptance patterns were similar between stink bug species, our results suggest a greater potential for parasitoid development in H. halys eggs compared to the native pentatomids. During host-range testing, we detected field populations of T. japonicus at 11 sites in Portland, OR, indicating an unintentional introduction and establishment. Further work is needed to characterize its nontarget activity and dispersal patterns in areas where H. halys causes economic damage in Oregon.