The brown marmorated stink bug (BMSB), Halyomorpha halys (Stal), is an invasive pentatomid introduced from Asia into the United States, Canada, multiple European countries, and Chile. In 2010, BMSB populations in the mid-Atlantic United States reached outbreak levels and subsequent feeding severely damaged tree fruit as well as other crops. Significant nuisance issues from adults overwintering inside homes were common. BMSB is a highly polyphagous species with a strong dispersal capacity and high reproductive output, potentially enabling its spread and success in invaded regions. A greater understanding of BMSB biology and ecology and its natural enemies, the identification of the male-produced aggregation pheromone, and the recognition that BMSB disperses into crops from adjacent wooded habitats have led to the development of behavior-based integrated pest management (IPM) tactics. Much is still unknown about BMSB, and continued long-term collaborative studies are necessary to refine crop-specific IPM pr...

Impact of the invasive brown marmorated stink bug in North America and Europe: History, biology, ecology, and management.

The brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), has emerged as a harmful invasive insect pest in North America and Europe in the 1990s and 2000s, respectively. Native to eastern Asia, this highly polyphagous pest (>120 different host plants) is spreading rapidly worldwide, notably through human activities. The increasing global importance of the pest suggests that more coordinated actions are needed to slow its spread and mitigate negative effects in invaded areas. Prevention of large-scale outbreaks will require accurate identification and effective mitigation tools to be rapidly developed and widely implemented. In this short review, we update the current distribution of H. halys, discuss potential geographic range expansion based on passive and active dispersal and provide insight on the economic, environmental and social impact associated with H. halys.

Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide

Trissolcus japonicus (Ashmead) is an Asian egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stal). 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 na tive 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.

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Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America

Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Stal) (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.

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

Halyomorpha halys was accidentally introduced into Switzerland around 2004 and has recently spread to several additional areas in Europe, with established populations documented in France, Italy, Greece and Hungary. To test whether generalist egg parasitoids of European Pentatomidae have the potential to control H. halys, and whether these could be as effective as their related Asian species, sentinel egg masses of H. halys and six native European pentatomids were exposed in two regions of Switzerland. Freeze-killed sentinel egg masses of H. halys were attacked by the platygastrid Trissolcus cultratus and the eupelmid Anastatus bifasciatus, whereas fresh egg masses of native Pentatomidae occassionally yielded four Scelionidae species: Trissolcus semistriatus, T. scutellaris, T. cultratus and Telenomus chloropus. In no-choice tests, T. chloropus and T. semistratus produced no offspring from fresh H. halys eggs, whereas T. cultratus and T. scutellaris were sporadically able to complete development. Stopping embryogenesis by freezing egg masses of H. halys at -80 °C enabled T. cultratus and T. semistriatus to produce a high number of offspring without influencing the behaviour of the parasitoids. In contrast to European platygastrids, the Asian parasitoids Trissolcus japonicus and T. cultratus (Chinese strain) caused significantly higher parasitism of fresh H. halys eggs. Differences in developmental success may be related to less efficient venom of European scelionids injected during oviposition. To date, A. bifasciatus is the only potential candidate for augmentaive biological control of H. halys in Europe as it was the only European parasitoid capable of consistent, successful development on fresh H. halys eggs.

Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe?

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$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.

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

Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys

The brown marmorated stink bug, Halyomorpha halys (Stal), 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.

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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.

Ashley L. Jones

Papers

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

Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys

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.