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.     

The potential global distribution of the brown marmorated stink bug, <Emphasis Type="Italic">Halyomorpha halys</Emphasis>, a critical threat to plant biosecurity

The brown marmorated stinkbug, Halyomorpha halys is a highly polyphagous invasive insect, which has more than 300 reported hosts, including important horticultural crops. It has spread to every Northern Hemisphere continent, most recently to Europe. Whilst there have been no reports of incursions into Southern Hemisphere countries, there have been many interceptions associated with trade and postal goods. We modelled the potential distribution of H. halys using CLIMEX, a process-oriented bioclimatic niche model. The model was validated with independent widespread distribution data in the USA, and more limited data from Europe. The model agreed with all credible distribution data. The few exceptions in the distribution dataset appeared to be transient observations of hitchhikers, or were found at the edge of the range, in regions with topographic relief that was not captured in the climatic datasets used to fit and project the model. There appears to be potential for further spread in North America, particularly in central and southern states of the USA. In Europe, there is substantial potential for further spread, though under historical climate the UK, Ireland, Scandinavia and the Baltic states of Estonia, Lithuania and Latvia appear not to be at risk of establishment of H. halys. In the Southern Hemisphere, regions with moist tropical, sub-tropical, Mediterranean and warm-temperate climates appear to be at substantial risk on each continent. The threats are greatest in prime horticultural production areas.     

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.     

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.     

<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.     

Seasonal parasitism and host specificity of <Emphasis Type="Italic">Trissolcus japonicus</Emphasis> in northern China

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.     

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.     

Pentatomid host suitability and the discovery of introduced populations of <Emphasis Type="Italic">Trissolcus japonicus</Emphasis> in Oregon

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.     

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.     

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.     

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.     

Enzymatic saccharification and ethanol production of <Emphasis Type="Italic">Acacia mangium</Emphasis> and <Emphasis Type="Italic">Paraserianthes falcataria</Emphasis> wood,and <Emphasis Type="Italic">Elaeis guineensis</Emphasis> trunk

We examined the saccharification and fermentation of meals from Acacia mangium wood, Paraserianthes falcataria wood, and Elaeis guineensis trunk. The levels of enzymatic hydrolysis of cellulose and ethanol production were highest for P. falcataria wood and lowest for A. mangium wood. Ultrasonication pretreatment of meal further increased the rates of hydrolysis and ethanol production in meal from P. falcataria wood. Through this pretreatment, hemicelluloses (xylan and xyloglucan) and cellulose were released in the meal from P. falcataria wood. Loosening of hemicellulose associations can be expected to make P. falcataria wood more useful for bioethanol production.     

Biomass and nutrient allocation to aboveground components in fertilized <Emphasis Type="Italic">Eucalyptus saligna</Emphasis> and <Emphasis Type="Italic">E. urograndis</Emphasis> plantations

The objective of this study was to evaluate biomass allocation and nutrient pools in aboveground biomass components in 18-month-old plantations of Eucalyptus saligna and E. urophylla × E. grandis (i.e. E. urograndis) in Brazil. The plantations were established by pulp companies in a large area comprising three soil types (Acrisols, Vertisols and Leptosols) in the grassland biome in southern Brazil, and an operational regime of planting and maintenance fertilization was used to ensure full availability of nutrients. Vertisols showed the highest availability of soil nutrients, and the P and Ca concentrations in aboveground biomass were also highest in this type of soil. The nutritional status of both species indicates great consumption of nutrients, particularly of P, K and Ca. At this early age, canopy biomass components still made the largest relative contribution, although debarked stem biomass already accounted for 41.5% and 37.4 of total aboveground biomass in E. saligna, and E. urograndis, respectively. Nutrient concentrations in biomass components were similar across species. For all macronutrients, except Ca and Mg, the concentration gradient followed the order wood < bark < branches < leaves. For all micronutrients, except Cu, the concentration gradient followed the order wood < branches ≈ bark < leaves. At the plantation stage studied, i.e. before canopy closure, the importance of the components as nutrient pools followed the order leaves > branches > wood > bark. The branches hold the majority of Ca reserves in biomass and are a very important pool of Mg, K, P and B. The bark makes a small contribution to total biomass, but stores a similar amount of Ca as leaves, being the second major pool after the branches. Comparison of the nutrients supplied by fertilization and the amounts stored in soil and aboveground indicates that the operational dose should be adjusted to each type of soil after further experimental fertilizer trials, as the supply of N and P appears to be too high, particularly for Vertisols. This is leading to the immobilization of P in biomass components that are not of importance in the biological or biochemical nutrient cycles, thus increasing the risk of larger exports of P during biomass removal.     

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.     

Patterns of niche filling and expansion across the invaded ranges of <Emphasis Type="Italic">Halyomorpha halys</Emphasis> in North America and Europe

Studies of realized niche shift and model transferability in alien species usually ignore the potential effects of source populations and different invaded-range environments on niche lability. We incorporate our detailed knowledge of the native-range source populations and global introduction history of brown marmorated stink bug (Halyomorpha halys) to examine intraspecific variation in realized niche expansion and unfilling, and to investigate how niche modelling approaches are affected by that variation. Realized niche dynamics of H. halys were analyzed using an ordination method, ecological niche models (ENMs), and occurrence records from (1) East Asia, (2) North America, (3) Europe, (4) native-range source populations for North America and Europe introductions, and (5) global range. Patterns of niche filling and expansion were observed across the invaded ranges of H. halys in North America and Europe: niche unfilling (42.7 %) and expansion (0.0 %) in North America, and unfilling (80.5 %) and expansion (28.0 %) in Europe. Some invasive populations have expanded into climatically novel areas in central Europe. Results presented here provide evidence that H. halys has not yet occupied all suitable climatic habitats in North America and Europe that resemble its native range, and the central USA and most parts of Europe appear to be most at risk of H. halys spread in near future. When realized niche shifts dominated by niche unfilling, fully capturing species’ requirement by basing ENMs on native range may be more important for accurate invasion forecasts than non-native models. Caution is warranted when using the source population to estimate invasion potential.     

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     

Natural biological control of <Emphasis Type="Italic">Halyomorpha halys</Emphasis> by native egg parasitoids: a multi-year survey in northern Delaware

Halyomorpha halys (Stål) is a highly polyphagous plant pest native to eastern Asia. Since its accidental introduction to the USA in the mid-1990s, it has spread across North America and caused serious economic damages. Chemical control has been a widely applied management strategy which is not sustainable on a long-term basis. A nine-year survey using sentinel and naturally laid H. halys was conducted to investigate the extent of natural biological control by parasitoids in managed and non-managed landscapes in northern Delaware, USA. Naturally laid egg masses of native pentatomids were collected to compare the resident parasitoid complex to the one attacking H. halys eggs. Mean parasitism rates of sentinel eggs were below 6% in any given year of the survey with a grand mean of 1.79%. Parasitism of naturally laid H. halys eggs was higher than that of sentinel eggs, but there was no significant difference in parasitism between years and the grand mean was 4.31%. Parasitoid species richness on sentinel and naturally laid H. halys eggs was similar but both were lower than the richness on native pentatomid eggs. H. halys eggs were parasitized by eight species in the genera Anastatus, Trissolcus, Telenomus, and Ooencyrtus. The level of parasitism by native egg parasitoids is insufficient to provide long-term control of H. halys. Trissolcus japonicus (Ashmead), an Asian egg parasitoid that has been recovered in the USA in several locations since 2014, may be the most promising candidate for long-term biological control of H. halys.