Possible coexistence of native and exotic parasitoids and their impact on control of <Emphasis Type="Italic">Halyomorpha halys</Emphasis>

Introduction of exotic natural enemies for biological control of invasive pests may disrupt existing ecological interactions, which may influence the outcome of biological control introductions. The interactions between Asian egg parasitoids, proposed as classical biological control agents of the highly polyphagous invasive pest Halyomorpha halys (Stål), and parasitoids native to the introduced area are largely unknown. Therefore, adult and larval interspecific competition between the exotic Trissolcus japonicus (Ashmead) and the European Anastatus bifasciatus (Geoffroy) was assessed (1) by observing aggressive interactions between adults of the two species following parasitization and (2) by providing each parasitoid species with previously parasitized H. halys egg masses at various time intervals. The results suggest that T. japonicus and A. bifasciatus engage in counterbalance competition, with the former being a superior extrinsic competitor (egg guarding and aggressiveness) and the latter being a superior intrinsic competitor (successful development from multiparasitized eggs of all ages). We suggest that the presence of T. japonicus is unlikely to have a negative impact on A. bifasciatus, and that those two species can coexist and potentially act synergistically in the biological control of H. halys.     

Chemical ecology of <Emphasis Type="Italic">Halyomorpha halys</Emphasis>: discoveries and applications

There have been notable and significant advances in elucidating the chemical ecology of the invasive Halyomorpha halys (Hemiptera: Pentatomidae), brown marmorated stink bug. This highly destructive and polyphagous pest is originally from Korea, China, and Japan, but was accidentally introduced into North America and Europe. Prior to its invasion into these regions, little was known about its chemical ecology. However, since then, researchers have identified and synthesized its aggregation pheromone, documented its synergism with the pheromone of another Asian stink bug, Plautia stali, developed monitoring traps of various designs, and lures with reliable attractants have become commercially available. Furthermore, plant volatiles have been shown to have attractive, neutral, and repellent effects on attraction and retention of H. halys, and H. halys-derived volatiles have been shown to play a role in recruiting natural enemies. Finally, management strategies based on pheromone-based technology have been evaluated, including insecticide applications based on a cumulative threshold of adult captures in pheromone-baited traps, and the use of intensively baited trees in an attract-and-kill strategy to manage this pest. This review summarizes the available literature on the chemical ecology of H. halys and concludes with several research areas that should be explored in future research.     

<Emphasis Type="Italic">Vicia faba</Emphasis> plants respond to oviposition by invasive <Emphasis Type="Italic">Halyomorpha halys</Emphasis> activating direct defences against offspring

The invasive stink bug Halyomorpha halys is established in many European and American agro-ecosystems, where it causes severe crop losses. Potential control measures might include enhancement of plant defences. When attacked by herbivorous insects that oviposit on it, the plant may respond by priming direct defences, which might affect the development of future brood. Halyomorpha halys attacks numerous plant species in the invaded areas. Here, we investigated whether Vicia faba plants challenged by H. halys females can impair the development of its offspring through the activation of induced direct defences. We measured the weight and dimension of nymphs that developed on oviposition-experienced plants after 7 and 17 days from hatching. Nymphs that developed on oviposition-experienced plants weighed less compared to those that developed either on control plants or on plants solely subjected to H. halys feeding, and third instars showed shorter dimensions (tibia length). In addition, when oviposition-experienced plants were attacked by nymphs, higher and more rapid expression of two jasmonic acid-dependent genes (cysteine proteinase inhibitor gene and NAI1) was detected, possibly due to a mechanism of priming. Increased expression of the salicylic acid-responsive PR1 gene was also detected in egg-experienced plants, although the response was delayed compared to JA-dependent genes. Our results suggest that V. faba plants recognize H. halys oviposition as a warning signal and pre-activate defences against future nymphal herbivory.     

Review of the chemical control research on <Emphasis Type="Italic">Halyomorpha halys</Emphasis> in the USA

The invasive brown marmorated stink bug Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) has become a serious economic pest in parts of the USA, and control tactics are often needed in order to avoid crop losses in tree fruit and other crops. Chemical control is usually the most effective and efficient tactic for preventing damage in crops. Researchers have tested a wide range of insecticides using laboratory and field experiments to determine the best options for H. halys control in the USA. This review summarizes that work and describes current practices with regard to insecticide options for H. halys.     

Predatory ability of the ant <Emphasis Type="Italic">Crematogaster scutellaris</Emphasis> on the brown marmorated stink bug <Emphasis Type="Italic">Halyomorpha halys</Emphasis>

The pest Halyomorpha halys is a recent example of severe worldwide biological invasion. In Italy, after the first detection in 2012, it has rapidly spread and economic damage has already been reported in commercial fruit orchards, eliciting enormous concern for Italian agricultural production. As a long-term solution, biological control investigations are focusing on the potential of natural antagonists, such as generalist predators, in the invaded areas. Due to their biology, ecology and behavior, ants represent one such generalist predator potentially suitable for inflicting mortality on H. halys. In this research, Crematogaster scutellaris was used as a study model. Specifically, the effect of ant predatory behavior on the survival of all H. halys pre-imaginal stages was tested in the laboratory environment. The results suggest that C. scutellaris has a significant predatory impact on all H. halys pre-imaginal stages except for eggs. The reduction of survivorship is between 95 and 85% for instars 1 and 2 and between 38 and 52% for instars 3, 4 and 5. The different levels of predation success suggest that these ants could act as useful generalist predators when associated with other antagonists and/or other control strategies. Although further field investigations are needed, the potential of ants as biocontrol agents of invasive species in agroecosystems deserves consideration in integrated pest management programs.     

Behavioral responses of the egg parasitoid <Emphasis Type="Italic">Trissolcus japonicus</Emphasis> to volatiles from adults of its stink bug host, <Emphasis Type="Italic">Halyomorpha halys</Emphasis>

Halyomorpha halys, originating from East Asia, has become an important agricultural pest in northern temperate regions since its accidental introduction into North America in the mid-1990s and Europe in 2007. Trissolcus japonicus is the predominant egg parasitoid of this pest in its native range. Here, we tested the hypothesis that T. japonicus uses volatiles associated with H. halys adults during host location. The effects of these volatile compounds on H. halys adults were also assessed. Chemical analysis with GC-MS and electrophysiological analysis with GC-EAD revealed the presence of two bioactive volatile compounds from H. halys adults, n-tridecane and (E)-2-decenal. In the Y-tube assays, female T. japonicus were attracted by n-tridecane but strongly repelled by (E)-2-decenal. Furthermore, host searching time of female T. japonicus was significantly reduced when an H. halys egg mass was treated with n-tridecane and prolonged when treated with (E)-2-decenal or a mixture of (E)-2-decenal and n-tridecane. Male H. halys were significantly attracted by n-tridecane, whereas females had no response to this compound in the Y-tube assays. (E)-2-Decenal strongly repelled male and female H. halys in the Y-tube assays. We discuss the multifunctional kairomonal and other possible roles of these semiochemicals at different trophic levels in the context of intra- and inter-specific chemical communication, in the H. halys–T. japonicus system.     

<Emphasis Type="Italic">Halyomorpha halys</Emphasis>, a serious threat for hazelnut in newly invaded areas

Following its first detection, Halyomorpha halys has become a key pest in many crops in NW Italy. In this area, one of the most important crops is hazelnut, in which the species can cause severe damage through feeding on nuts. Therefore, semi-field trials were carried out in NW Italy to compare the harmfulness of H. halys with that of the local hazelnut bug species, such as Gonocerus acuteangulatus, Nezara viridula, and Palomena prasina. Additionally, a 2-year field survey was conducted in hazel groves in NW Italy and W Georgia, another important hazelnut cropping area, to assess the presence and abundance of the new invasive species and to evaluate the damage at harvest. Monitoring was carried out by plant beating and by commercial traps throughout the growing season. In semi-field trials, H. halys was the most harmful species, causing the highest damage in kernels, and was able to survive and reproduce at higher rates. During field surveys in NW Italy, H. halys was sampled in groves late in the season in 2015 and, with higher populations, throughout the season in 2016. In W Georgia, bug population levels consistently increased in the 2-year period, resulting in a significant increase in damage at harvest in 2016. A similar trend is hence expected also in NW Italy in the following years. Moreover, data on individuals collected in different points of the hazelnut groves confirmed the border-driven behavior of this pest, leading to consideration of potential integrated pest management solutions.     

Development and fecundity of <Emphasis Type="Italic">Trissolcus japonicus</Emphasis> on fertilized and unfertilized eggs of the brown marmorated stink bug, <Emphasis Type="Italic">Halyomorpha halys</Emphasis>

Halyomorpha halys, the brown marmorated stink bug, is a serious agricultural and horticultural pest native to East Asia, which became an invasive pest in northern temperate parts of other regions in the mid-1990s. Trissolcus japonicus is a dominant egg parasitoid of H. halys in its native range. In this paper, we investigated mating, oviposition and fecundity of both virgin and mated females of H. halys. Virgin H. halys females produced unfertilized eggs, while mated females produced fertilized eggs, but mating states of adult females did not affect the number of eggs produced. We further compared the development and fecundity of T. japonicus on fertilized or unfertilized eggs of various ages. Fertilized eggs were tested continuously for up to 5 days (time to hatch), while unfertilized eggs were tested for up to 11 days (time to egg collapse). The fertilization status of the host egg had a significant effect on the development, emergence success, and sex ratio of T. japonicus progeny. A small increase in development time was observed for T. japonicus in fertilized eggs, fewer T. japonicus emerged from fertilized eggs than unfertilized eggs, and the proportion of female progeny was lower on fertilized eggs. The age of host eggs also significantly affected the development rate and fecundity of T. japonicus, with unfertilized eggs becoming more favorable than fertilized eggs as egg age increased. In summary, unfertilized H. halys eggs were better suited for T. japonicus development and fecundity, indicating their potential use in T. japonicus mass rearing.     

Field surveys of egg mortality and indigenous egg parasitoids of the brown marmorated stink bug, <Emphasis Type="Italic">Halyomorpha halys</Emphasis>, in ornamental nurseries in the mid-Atlantic region of the USA

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

Successful <Emphasis Type="Italic">Agrobacterium</Emphasis>-mediated transformation of <Emphasis Type="Italic">Populus tomentosa</Emphasis> with apple <Emphasis Type="Italic">SPDS</Emphasis> gene

The problem of salinized soils has become one of the most serious constraints to agricultural and forest productivity. With the purpose of enhancing salt stress tolerance of Populus tomentosa, we transformed this tree species with spermidine synthase （SPDS） genes derived from an apple by an Agrobacterium-mediated method. Four transgenic clones were confu＇med by PCR and Southern blot analysis. As well, the expression of introduced SPDS genes was analyzed by real-time quantitative PCR.     

Host specificity of Asian parasitoids for potential classical biological control of <Emphasis Type="Italic">Drosophila suzukii</Emphasis>

The Asian spotted wing drosophila, Drosophila suzukii, has recently become a serious pest of soft fruits in Europe. Classical biological control through the introduction of larval parasitoids from its native range in Asia is presently being considered. However, host specificity of potential biological control agents has to be determined to avoid releasing species that may have unintended non-target impacts. Larvae of six different European non-target fly species and the target D. suzukii were exposed either on diet or blueberries to three Asian larval parasitoids, Asobara japonica, Leptopilina japonica, and Ganaspis cf. brasiliensis, and one European species, Leptopilina heterotoma. Asobara japonica showed the lowest specificity, attacking and developing in all Drosophilidae. Leptopilina japonica successfully parasitized two non-target Drosophilidae, D. melanogaster and D. subobscura, with one singly progeny emerging from D. immigrans. Ganaspis cf. brasiliensis had the highest level of specificity but variations occurred between two geographical populations tested. A Japanese population was strictly specific to D. suzukii, whereas another population from China parasitized D. suzukii, D. melanogaster and sporadically D. subobscura. The European L. heterotoma successfully developed in D. melanogaster, D. subobscura and occasionally in D. immigrans, but nearly all eggs and larvae in D. suzukii were encapsulated. These results show that Ganaspis cf. brasiliensis is the species with the highest potential for biological control, but more studies are needed on its taxonomic status and the existence of biotypes or cryptic species varying in their specificity before field releases can be conducted in Europe.     

Pheromone-based decision support tools for management of <Emphasis Type="Italic">Halyomorpha halys</Emphasis> in apple orchards: development of a trap-based treatment threshold

The invasive brown marmorated stink bug, Halyomorpha halys (Stål), has become a serious pest in mid-Atlantic apple orchards. Because no decision support tools exist for H. halys management, calendar-based insecticide applications have been the only successful technique for mitigating H. halys injury in orchards. Following the identification of the two-component aggregation pheromone of H. halys, we conducted a study to determine whether biological information generated by traps baited with this pheromone and pheromone synergist could be used to make management decisions. In this study, experimental apple orchards were treated with a H. halys-targeted insecticide only when a predetermined cumulative threshold of either 1, 10, or 20 adults per trap was reached. Once threshold was reached, two alternate row middle sprays 1 week apart were triggered and the threshold was reset. For comparison, some orchards were also subjected to a weekly alternate row middle spray or left untreated as controls. At harvest, significantly less fruit injury was observed when treated weekly or using a threshold of 1 or 10 H. halys adults per trap to trigger insecticide applications. Orchards treated using a cumulative threshold of 20 adults per trap or when left unsprayed had significantly higher fruit injury. In addition, insecticide applications were reduced by 40% using a threshold of 10 adults per trap. Our results suggest that baited pheromone traps can be used as decision support tools to trigger insecticide applications when needed to mitigate risk and effectively manage H. halys in apple orchards.     

Laboratory rearing of <Emphasis Type="Italic">Halyomorpha halys</Emphasis>: methods to optimize survival and fitness of adults during and after diapause

Laboratory colonies are necessary to conduct year-round research on the invasive brown marmorated stink bug, Halyomorpha halys (Stål), a severe agricultural and nuisance pest in the USA. When adults are collected in the fall to either start or supplement colonies, they require a period of cold storage before they resume sexual development and egg production. There is a lack of understanding of how to collect and store diapause-triggered adults in the laboratory. A series of experiments in 2013–2015 assessed survival and fecundity of stink bugs collected from different locations and stored under different temperatures and durations. We found that a minimum of 7 weeks is necessary to break diapause and that a substantial proportion of adults can survive when stored at constant 9 °C, even for periods longer than needed to terminate diapause. Adults survived significantly better at 6 and 9 °C than at 3 °C in storage for 7 weeks. Longer durations up to 34 weeks in storage reduced adult survival and significantly affected survival rates, timing of first egg laying, and overall fecundity. Location where adults were collected at overwintering sites in the fall had a significant impact on survival in cold storage and colony performance. Adults collected from soybean fields in mid-September and fed in the laboratory for 2 weeks before storage had lower survival than adults collected in October at aggregation sites and stored immediately. The food sources available to H. halys adults at collection locations for nutrition and sequestration of sufficient energy reserves going into diapause are discussed.     

Insecticidal properties of <Emphasis Type="Italic">Thymus persicus</Emphasis> essential oil against <Emphasis Type="Italic">Tribolium castaneum</Emphasis> and <Emphasis Type="Italic">Sitophilus oryzae</Emphasis>

Red flour beetle Tribolium castaneum (Herbst) and rice weevil Sitophilus oryzae (L.) are considered to be the major insect pests in storage. Essential oils from aromatic plants are recognized as proper alternatives to fumigants. Thymus persicus (Ronniger ex Rech. f.) is one of these plants that have medicinal properties and is indigenous to Iran. The essential oil was obtained from aerial parts of the plant and analyzed by GC and GC–MS. Carvacrol (44.69%) and thymol (11.05%) were the major constituents of the oil extracted. In this experiment, fumigant toxicity of the essential oil was studied against T. castaneum, S. oryzae at 27 ± 1°C and 60 ± 5% RH in dark condition. The adult insects were exposed to the concentrations of 51.9, 111.1, 207.4 and 370.4 μl/l air to estimate median lethal time (LT₅₀) values. The fumigant toxicity was increased in response to increased essential oil concentrations. The LT₅₀ values at the lowest and the highest concentrations tested were ranged from 28.09 to 13.47 h for T. castaneum, and 3.86 to 2.30 h for S. oryzae. It was found that S. oryzae adults were much more susceptible to the oil than T. castaneum. After 24 h of exposure, the LC₅₀ values (95% fiducial limit) for T. castaneum and S. oryzae were estimated to be 236.9 (186.27–292.81) and 3.34 (2.62–4.28) μl/l air, respectively. These results suggest that T. persicus essential oil merits further study as potential fumigant for the management of these stored-product insects.     

Bioremediation of CCA-treated wood by brown-rot fungi <Emphasis Type="Italic">Fomitopsis palustris</Emphasis>, <Emphasis Type="Italic">Coniophora puteana</Emphasis>, and <Emphasis Type="Italic">Laetiporus sulphureus</Emphasis>

This study evaluated oxalic acid accumulation and bioremediation of chromated copper arsenate (CCA)-treated wood by three brown-rot fungi Fomitopsis palustris, Coniophora puteana, and Laetiporus sulphureus. The fungi were first cultivated in a fermentation broth to accumulate oxalic acid. Bioremediation of CCA-treated wood was then carried out by leaching of heavy metals with oxalic acid over a 10-day fermentation period. Higher amounts of oxalic acid were produced by F. palustris and L. sulphureus compared with C. puteana. After 10-day fermentation, oxalic acid accumulation reached 4.2 g/l and 3.2 g/l for these fungi, respectively. Fomitopsis palustris and L. sulphureus exposed to CCA-treated sawdust for 10 days showed a decrease in arsenic of 100% and 85%, respectively; however, C. puteana remediation removed only 18% arsenic from CCA-treated sawdust. Likewise, chromium removal in F. palustris and L. sulphureus remediation processes was higher than those for C. puteana. This was attributed to low oxalic acid accumulation. These results suggest that F. palustris and L. sulphureus remediation processes can remove inorganic metal compounds via oxalic acid production by increasing the acidity of the substrate and increasing the solubility of the metals.An erratum to this article can be found at     

<Emphasis Type="Italic">Bursaphelenchus mucronatus</Emphasis> (Nematoda: Aphelenchoididae) vectored by <Emphasis Type="Italic">Monochamus </Emphasis><Emphasis Type="Italic">urussovi</Emphasis> (Coleoptera: Cerambycidae) in Hokkaido,Japan

Bursaphelenchus mucronatus Mamiya et Enda has been recovered for the first time from adults of the cerambycid beetle, Monochamus urussovi (Fischer), in Hokkaido, Japan. The nematode was also recovered from the inner bark of Picea jezoensis (Siebold et Zuccarini) Carrière and Abies sachalinensis (Fr Schmidt) Masters infested with M. urussovi larvae. PCR–RFLP analysis indicated that B. mucronatus in Hokkaido is the European type.     

Establishment of native <Emphasis Type="Italic">Eucalyptus pauciflora</Emphasis> and exotic <Emphasis Type="Italic">Eucalyptus nitens</Emphasis> on former grazing land

The success of tree plantings in agricultural landscapes within dry and variable rainfall regions is often below expectations. The aims of this study were to investigate techniques for establishing a local native species (Eucalyptus pauciflora) and an exotic species (E. nitens) in the Midlands of Tasmania, a tree-denuded region that has been grazed for over 100 years in Australia. We established trials at the Sorrel Springs and Woodland Park properties. We compared six establishment techniques: control; understorey nurse planting; spot burn; mulch; tree-guard and; self-watering tree-guard. Three months, 1 and 6 years after planting we measured tree height, health index and mortality. At Sorrell Springs tree-guarded treatments had greater height than other treatments at year one, but there were no effects of treatment at year six on height, health or mortality. At Woodland Park mulch, burn and tree-guarded treatments had greater height 1 and 6 years after planting. At year six tree-guarded treatments had lower mortality than other treatments. At Sorrell Springs height of E. nitens was greater than E. pauciflora at year one but not at year six. At Woodland Park height of E. nitens was generally greater at year six but having almost double the incidence of mortality relative to E. pauciflora. We conclude that expensive tree-guarding is only warranted where high browse pressure is expected and that on such sites species with tough leaves that are resistant to browsing should be considered. Further that in environments marginal for growing trees, best practice establishment technique is generally as effective as additional treatments of understorey nurse planting, spot burning or mulching.     

Toxicity of synthetic and biological insecticides against adults of the <Emphasis Type="Italic">Eucalyptus</Emphasis> snout-beetle <Emphasis Type="Italic">Gonipterus</Emphasis><Emphasis Type="Italic">scutellatus</Emphasis> Gyllenhal (Coleoptera: Curculionidae)

Toxicity by contact and by ingestion of lufenuron, flufenoxuron, lambda (λ)-cyhalothrin, cypermethrin, thiamethoxam and five entomopathogenic insecticides (three formulations of Beauveria bassiana, a compound containing spores of Metarhizium anisopliae var. acridum, and a mixture of Brevibacillus laterosporus, Bacillus licheniformis and Bacillus chitinosporus) were evaluated on adults of the Eucalyptus snout-beetle Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae) under laboratory conditions. By contact, entomopathogenic fungus B. bassiana EC and the pyrethroid λ-cyhalothrin exhibited the highest efficiency, achieving 100 and 97.5% mortality, respectively. By ingestion, the highest mortality was obtained by B. bassiana EC (100%) and thiamethoxam (95%). Flufenoxuron and lufenuron, bacteria mixture and M. anisopliae showed a weak toxicity. Furthermore, we found a sex-biased mortality, being males more affected. Due to the good performance and low risk to humans and environment, B. bassiana EC (strain PPRI 5339) appears to be the most promising product to promote an IPM programme in South Africa.     

Introduced <Emphasis Type="Italic">Tuber aestivum</Emphasis> replacing introduced <Emphasis Type="Italic">Tuber melanosporum</Emphasis>: a case study

A Tuber melanosporum plantation established in 1994/1995 on Kibbutz Bar’am (in the Upper Galilee, Israel) gradually lost its T. melanosporum mycorrhiza. In 1999, T. aestivum inoculated seedlings were inadvertently introduced into the plantation to fill the gaps between trees. A single T. melanosporum fruit body was found in 1999. Although no truffles were found after 1999 and until 2009, in that year and in 2010, truffles were collected. Morphological and molecular analyses proved these to be T. aestivum. Thus, the intentionally introduced T. melanosporum mycorrhiza was replaced by that of another introduced mycorrhizal fungus, T. aestivum. Local oak species produced higher yields compared to introduced host species known to be good T. melanosporum plant symbionts. The yield was comparable to that reported for young commercial orchards, but the fruiting season was earlier than in Europe.