Kim A. Hoelmer

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

European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America

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.

Multifaceted determinants of host specificity in an aphid parasitoid

We consider the possibility of an extensive invasional meltdown occurring in central North America involving eleven Eurasian species. The scenario begins with the potential co-facilitation between the European earthworm Lumbricus terrestris and European buckthorn, Rhamnus cathartica. Once introduced, European buckthorn has served as the overwintering host for two important invasive crop pests, oat crown rust, Puccinea coronata and the soybean aphid, Aphis glycines. The spread of R. cathartica itself may have been aided by seed dispersal by the European starling, Sturnus vulgaris, and the presence of L. terrestris has likely facilitated the invasion of Bipalium adventitium, an Asian predatory flatworm that specializes on earthworms. Beyond this, the soybean aphid is consumed by a number of introduced species, including the lady beetle Harmonia axyridis, the ground beetle Agonum muelleri and the parasitoid Aphelinus certus. We hypothesize that the presence of soybean aphid increases regional abundances of these species. We discuss both the evidence for this multi-species invasional meltdown scenario and potential implications of meltdown dynamics for invasive species management. The particular management issues that we discuss are: (1) opportunities for managing multiple invasive species simultaneously by targeting facilitator species, and (2) implications of meltdown dynamics for biological control introductions against the soybean aphid.

Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world

The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.

Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance.

After its arrival in 2008, the Spotted Wing Drosophila (SWD), Drosophila suzukii, has emerged as a harmful invasive insect pest in North America and Europe. This highly polyphagous pest is a major threat to many economically important fruit crops and is also known to develop on a wide variety of natural host plants. In Asia, Europe and North America, different control measures are applied against SWD, such as chemical, biological, and cultural control. Current controls of SWD rely primarily on the application of insecticides, but cultural management tactics such as sanitation and the use of nets provide a good alternative in some crops. Biological control measures, such as conservation of existing natural enemies in invaded areas, introduction of specialized larval parasitoids from Asia for classical biological control and the use of indigenous parasitoids for augmentative control, are currently being investigated and may become an important management tool in the near future for an area-wide control of SWD.

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

The Asian parasitoid, Binodoxys communis (Gahan) (Hymenoptera: Braconidae), is a candidate for release against the exotic soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in North America. In this study, we examined preferences by B. communis for the different developmental stages of A. glycines and investigated consequences of these preferences for parasitoid fitness. We also determined to what extent aphid defensive behaviours mediate such preferences. We found that B. communis readily attacks and successfully develops in the different A. glycines developmental stages. Binodoxys communis development time gradually increased with aphid developmental stage, and wasps took longest to develop in alates. An average (+/-SE) of 54.01+/-0.08% of parasitized A. glycines alatoid nymphs transformed into winged adult aphids prior to mummification. No-choice assays showed a higher proportion of successful attacks for immature apterous A. glycines nymphs compared to adults and alatoid nymphs. Also, choice trials indicated avoidance and lower attack and oviposition of adults and alatoid nymphs. The different aphid stages exhibited a range of defensive behaviours, including body raising, kicking and body rotation. These defenses were employed most effectively by larger aphids. We discuss implications for the potential establishment, spread and biological control efficacy of A. glycines by B. communis in the event that it is released in North America.

Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys.

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.

Cryptic Species of Parasitoids Attacking the Soybean Aphid (Hemiptera: Aphididae) in Asia: Binodoxys communis and Binodoxys koreanus (Hymenoptera: Braconidae: Aphidiinae)

Identifying the origin of a biological invasion has important applications to the effective control of the invaders. This is more critical for invasive agricultural pests that cause severe economic losses. The brown marmorated stink bug, Halyomorpha halys, originally from East Asia, has become a principal agricultural pest in the US since its first detection in Pennsylvania in 1996. This species is responsible for crop failures on many mid-Atlantic farms and current control efforts rely on heavy insecticide applications because no other options are available. To examine the genetic diversity and identify the source region of the US introductions, we sequenced portions of the mitochondrial cytochrome c oxidase subunit II gene, 12S ribosomal RNA gene and control region in populations from the US, China, South Korea and Japan. We detected high genetic divergence among native populations and traced the origin of US H. halys to the Beijing area in China. We observed much lower genetic diversity in exotic compared to native populations—two mitochondrial haplotypes in 55 US specimens versus 43 haplotypes in 77 native specimens. A single introduction of small propagule size matches the invasion history in the US. For the effective control of the US population, we suggest that surveys on egg parasitoids and insecticide resistance in natives should focus on the Beijing area in China.

Complete mitochondrial genome of brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), and phylogenetic relationships of hemipteran suborders

ABSTRACT Collections of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in South Korea yielded specimens that were originally identified as Binodoxys communis (Gahan) (Hymenoptera: Braconidae). We report here on laboratory studies indicating that this population is actually a previously unknown species of Binodoxys. Four classes of comparisons were made between the Korean population and a Chinese population that also had been identified as B. communis. The comparisons included 1) mating trials coupled with behavioral observations and spermathecal examinations, 2) assessment of nucleotide divergence at two mitochondrial and two nuclear gene loci, 3) patterns of host use, and 4) reassessment of morphological characters. These studies revealed premating reproductive isolation of the two populations and minor nucleotide differences in mitochondrial cytochrome oxidase I sequences and nuclear internal transcriber spacer 1 sequences, providing strong indications that they are different species. Subtle morphological differences also were discovered that confirmed that the Chinese population corresponds to B. communis, whereas the Korean population does not. We propose the name Binodoxys koreanus StarÝ, sp. n. for the Korean population. The two species exhibited similar host ranges in the laboratory, the most notable exception being that B. koreanus, sp. n. is better able to develop in a population of Aphis craccivora Koch that harbors the bacterial endosymbiont Hamiltonella defensa Moran, which seems to strongly interfere with the development of B. communis. We discuss the implications of our results for biological control introductions against the soybean aphid in North America.

A survey of fruit-feeding insects and their parasitoids occurring on wild olives, Olea europaea ssp. cuspidata, in the Eastern Cape of South Africa

The newly sequenced complete mitochondrial genome of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a circular molecule of 16,518 bp with a total A+T content of 76.4% and two extensive repeat regions in A+T rich region. Nucleotide composition and codon usage of H. halys are about average when compared with values observed in 19 other published hemipteran mitochondrial genomes. Phylogenetic analyses using these 20 hemipteran mitochondrial genomes support the currently accepted hypothesis that suborders Heteroptera and Auchenorrhyncha form a monophyletic group. The mitochondrial gene arrangements of the 20 genomes are also consistent with our results.