Tara D. Gariepy

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

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

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.

A single-step multiplex PCR assay for the detection of European Peristenus spp., parasitoids of Lygus spp.

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.

Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland

Abstract Lygus Hahn (Hemiptera: Miridae) are serious pests of agricultural and greenhouse crops throughout North America. In Europe, bivoltine Peristenus Förster (Hymenoptera: Braconidae) species have a significant impact on Lygus populations. Release and establishment of European P. digoneutis Loan in Lygus lineolaris (Palisot de Beauvois) populations in northeastern USA has renewed interest in the intended liberation of European parasitoids for Lygus control in Canada. Accurate identification of natural enemies is the cornerstone of biological control but conventional methods for identifying Peristenus species and estimating parasitism rates rely on tedious and time-consuming dissection and rearing methods. The present study describes species-specific PCR primers for three species of Peristenus, and the use of a multiplex PCR assay to detect P. digoneutis and P. stygicus Loan eggs and larvae from Lygus rugulipennis Poppius nymphs. Results indicate that the primers amplify uniquely sized, species-specific PCR products for the three species and are capable of detecting single eggs in parasitized nymphs within 3 days post-parasitism. Using a multiplex PCR assay, the primers maintain specificity and sensitivity, and allow detection of each of the three species in a single reaction. Although molecular diagnostics have previously been used in the identification of parasitoids and estimation of parasitism rates, this is the first time a single-step multiplex PCR protocol has been described.

Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii.

Halyomorpha halys has recently established in countries outside of its Asian area of origin. In the North Eastern USA, this pest causes severe economic loss in agricultural crops. Breeding populations have been confirmed in Switzerland and Canada; however, their pathways of entry and genetic diversity remain unknown. To determine invasion pathways and source population(s), the diversity of specimens from Asia, North America, and Europe was investigated. Genetic diversity in Asia was higher than that in the Canada and Switzerland. Although three haplotypes were detected among Canadian H. halys, one haplotype dominated. In contrast, two out of three haplotypes were found frequently among Swiss samples. Based on molecular data and interception records it appears likely that H. halys in Canada is derived from the movement of established US populations. Further, North American populations likely originated from the Hebei/Beijing regions of China. The area of origin of the Swiss samples remains unclear. Although the dominant haplotype in Switzerland was consistent with Asian samples collected in the Hebei and Beijing provinces, it was not the dominant haplotype in these regions and further sampling is necessary to its confirm the distribution and abundance in the area of origin. The remaining two haplotypes were unique to Switzerland and no matches were found among our Asian samples. Interestingly, no haplotypes were shared between the North American and Swiss samples, indicating that the two invasions were separate and distinct events and did not result from the movement of goods and materials between USA and Europe.

A molecular diagnostic tool for the preliminary assessment of host-parasitoid associations in biological control programmes for a new invasive pest.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is a worldwide emerging pest of soft fruits, but its cold tolerance has not been thoroughly explored. We determined the cold tolerance strategy, low temperature thermal limits, and plasticity of cold tolerance in both male and female adult D. suzukii. We reared flies under common conditions (long days, 21°C; control) and induced plasticity by rapid cold-hardening (RCH, 1h at 0°C followed by 1h recovery), cold acclimation (CA, 5 days at 6°C) or acclimation under fluctuating temperatures (FA). D. suzukii had supercooling points (SCPs) between -16 and -23°C, and were chill-susceptible. 80% of control flies were killed after 1h at -7.2°C (males) or -7.5°C (females); CA and FA improved survival of this temperature in both sexes, but RCH did not. 80% of control flies were killed after 70 h (male) or 92 h (female) at 0°C, and FA shifted this to 112 h (males) and 165 h (females). FA flies entered chill coma (CTmin) at approximately -1.7°C, which was ca. 0.5°C colder than control flies; RCH and CA increased the CTmin compared to controls. Control and RCH flies exposed to 0°C for 8h took 30-40 min to recover movement, but this was reduced to <10 min in CA and FA. Flies placed outside in a field cage in London, Ontario, were all killed by a transient cold snap in December. We conclude that adult phenotypic plasticity is not sufficient to allow D. suzukii to overwinter in temperate habitats, and suggest that flies could overwinter in association with built structures, or that there may be additional cold tolerance imparted by developmental plasticity.

Occurrence and genetic diversity of new populations of Halyomorpha halys in Europe.

Evaluation of host–parasitoid associations can be tenuous using conventional methods. Molecular techniques are well placed to identify trophic links and resolve host–parasitoid associations. Establishment of the highly invasive brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), outside Asia has prompted interest in the use of egg parasitoids (Hymenoptera: Scelionidae) as biological control agents. However, little is known regarding their host ranges. To address this, a DNA barcoding approach was taken wherein general PCR primers for Scelionidae and Pentatomidae were developed to amplify and sequence >500‐bp products within the DNA barcoding region of the cytochrome oxidase I (COI) gene that would permit the identification of key players in this association. Amplification of DNA from Pentatomidae and Scelionidae was consistent across a broad range of taxa within these families, and permitted the detection of Scelionidae eggs within H. halys 1 h following oviposition. In laboratory assays, amplification and sequencing of DNA from empty, parasitized eggs was successful for both host (100% success) and parasitoid (50% success). When applied to field‐collected, empty egg masses, the primers permitted host identification in 50–100% of the eggs analysed, and yielded species‐level identifications. Parasitoid identification success ranged from 33 to 67% among field‐collected eggs, with genus‐level identification for most specimens. The inability to obtain species‐level identities for these individuals is due to the lack of coverage of this taxonomic group in public DNA sequence databases; this situation is likely to improve as more species are sequenced and recorded in these databases. These primers were able to detect and identify both pentatomid host and scelionid parasitoid in a hyperparasitized egg mass, thereby clarifying trophic links otherwise unresolved by conventional methodology.

Seasonal parasitism and host specificity of Trissolcus japonicus in northern China

Originating in East Asia, the brown marmorated stink bug, Halyomorpha halys, has established in North America and Europe where it has become an urban and agricultural pest. Although initial populations in Europe were only reported in Switzerland, H. halys has expanded its range to include areas in France, Greece, Hungary, and Italy. Analysis of a portion of the mitochondrial COI gene was used to evaluate the genetic diversity of these populations and to investigate the movement and spread of different COI haplotypes of this pest in Europe. A total of 9 haplotypes are now confirmed in Europe. Four of these haplotypes have not been previously reported elsewhere, and one of these haplotypes has not been previously reported in Europe but is known from Korea. The H. halys population in Greece was the most diverse, with 7 of the 9 haplotypes occurring in the area of collection. Haplotype H1, which is known from North America, Italy, and China, was also present in samples collected in France, Greece, Hungary, and Switzerland. In fact, the H1 haplotype was the dominant haplotype detected in Budapest, Hungary and also occurred frequently in the samples from Athens, Greece. Patterns of haplotype diversity indicate the movement of successful invasive populations to generate secondary invasions within Europe (‘bridgehead effect’), as well as the occurrence of multiple invasions from Asia. Scenarios regarding the movement and spread of particular haplotypes in Europe are discussed.

Bioclimatic analyses of distributions of a parasitoid Peristenus digoneutis and its host species Lygus spp. in Europe and North America.

The brown marmorated stink bug, Halyomorpha halys (Stål), native to China, Japan, and Korea, has emerged as a harmful invasive pest of a variety of crops in North America and Europe. The Asian egg parasitoid Trissolcus japonicus has been identified as the most promising agent for classical biological control of invasive H. halys populations. A 4-year study evaluated the fundamental and ecological host ranges of T. japonicus as well as its phenology and impact on H. halys populations in fruit orchards in its native range in northern China. In laboratory no-choice tests, developmental suitability of eight non-target host species for T. japonicus was demonstrated by the successful production of progeny on the majority (>85%) of non-target host species tested. In field-collected, naturally laid egg masses, T. japonicus was the most abundant parasitoid associated with H. halys and Dolycoris baccarum, but was also sporadically found in Plautia crossota. Furthermore, it was regularly reared from sentinel egg masses of Menida violacea, Arma chinensis, and Carbula eoa. The only species that did not support development in the laboratory and field was Cappaea tibialis. Besides the benefit of having a high impact on H. halys populations in Northern China, the risk assessment conducted in the area of origin indicates that native Pentatomidae in North America and Europe could be negatively impacted by T. japonicus. Whether the benefits of T. japonicus outweigh the possible risks will have to be evaluated based on the outcome of additional host range studies in the two invaded regions.

An exotic parasitoid provides an invasional lifeline for native parasitoids

1 Peristenus digoneutis Loan is a parasitoid of Lygus plant bugs, which was successfully introduced from Europe into North America in the 1980s for controlling native Lygus populations. Surveys confirmed that P. digoneutis populations have become established throughout eastern North America and that the spread of the parasitoid continues. For unknown reasons, previous releases of P. digoneutis in Western Canada were not successful. 2 A bioclimate (climex®; Hearne Scientific Software Pty Ltd, Australia) model for P. digoneutis in North America was developed, based on climate and ecological parameters, and then validated with actual distribution records. The current distribution of P. digoneutis in eastern North America was consistent with the predicted distribution. The model suggests that P. digoneutis will probably continue its spread westwards throughout the U.S.A. along the Great Lakes. 3 The southern distribution of P. digoneutis is expected to be limited by hot summer temperatures, whereas its northern range is limited by the number of Lygus host generations rather than cold stress. 4 Peristenus digoneutis has the potential to occur in the southern parts of the prairie ecozone of western Canada; however, Ecoclimatic Index values in the prairies indicate mainly marginal or unfavourable conditions, which may explain why earlier releases of P. digoneutis in Western Canada failed.