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.     

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.     

Seasonal parasitism of native egg parasitoids of brown marmorated stink bug (Halyomorpha halys) in Japan

Journal of Pest Science - The invasive, Halyomorpha halys (Hemiptera: Pentatomidae), is a severe economic insect pest native to East Asia. A strong effort has been made to identify natural egg...     

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.     

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.     

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.     

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.     

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.     

Phenology,life table analysis and temperature requirements of the invasive brown marmorated stink bug,Halyomorpha halys,in Europe

The invasive Halyomorpha halys was accidentally introduced into Switzerland around 2004 and has recently established in the neighbouring countries of France and Italy. To better understand the population dynamics of this pest in Europe, the phenology, reproductive biology and temperature requirements of Swiss H. halys populations were investigated. Overwintered adults became active in April, but peak oviposition was not observed before early July. Individual females laid on average 79 eggs (maximum of 160). The oviposition period lasted from mid-June to end of September. Eggs laid in August and September did not result in offspring due to the low temperatures in autumn. Under natural fluctuating temperatures, development from egg to adult lasted between 60 and 131 days. The first new generation of adults did not occur before mid-August when the photoperiod was already below 15 h, which likely initiated diapause and suppressed the reproductive activity of new generation adults. Under controlled conditions of 20, 25 and 30 °C, Swiss H. halys populations developed within 75.8, 42.3 and 33.2 days from egg to adult, respectively. No development was possible at or below 15 and at or above 35 °C. The number of degree days required for completion of development from egg to adult was 588.24 DD. Under semi-natural conditions, total mortality of Swiss H. halys populations was 86.7 % with a net reproductive rate of 5.69, indicating growing populations. In Switzerland, H. halys is univoltine, but if it continues to spread into the Mediterranean area two generations per year could be expected.     

<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.     

<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.     

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.     

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.     

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.     

Management Effects on Biomass and Foliar Nutritive Value of <Emphasis Type="Italic">Robinia pseudoacacia</Emphasis> and <Emphasis Type="Italic">Gleditsia triacanthos</Emphasis> f. <Emphasis Type="Italic">inermis</Emphasis> in Arkansas,USA

The browse potential of black locust (Robinia pseudoacacia L.) and thornless honey locust [Gleditsia triacanthos f. inermis (L.) Zabel] has not been adequately tested. Our objective was to determine effects of fertilization and pollarding on biomass and foliar nutritive value in separate studies of black locust and thornless honey locust in Arkansas, USA. Shoots were sampled monthly for two consecutive growing seasons in 2002 and 2003 to determine foliar, shoot, and total aboveground biomass, shoot basal diameter, and foliar nutritive value (crude protein and in vitro digestibility). Black locust yielded more foliar biomass when pollarded at 50 or 100 cm and fertilized with 600 kg P ha⁻¹, than at 5 cm with or without P, averaging 3.5 Mg dry matter ha⁻¹. Black locust foliar crude protein and in vitro dry matter digestibility ( ≤ 170 and 534 g kg⁻¹, respectively) decreased as leaves aged, but still met maintenance needs for beef cattle (Bos taurus L.). Thornless honey locust had little agronomic potential because of slow establishment, low foliar yield (330 kg ha⁻¹), and a 2% reversion to undesirable thorny phenotype. Black locust should be considered for livestock browse when drought induces semi-dormancy of herbaceous forages.     

Effects of <Emphasis Type="Italic">Verticillium nonalfalfae</Emphasis> on <Emphasis Type="Italic">Ailanthus altissima</Emphasis> and associated indigenous and invasive tree species in eastern Austria

The naturally occurring Verticillium nonalfalfae shows promise for biocontrol of the highly invasive Tree of Heaven (Ailanthus altissima), but might also bear a risk for non-target tree species. In this study, we conducted inoculations on potted seedlings of A. altissima as well as on eight indigenous and two invasive tree species associated with Tree of Heaven in Austria. Although vascular discolourations developed in all inoculated tree species, V. nonalfalfae was reisolated from Ailanthus and eight of the ten non-target-species, whereas typical disease symptoms and mortality only occurred on A. altissima. Results confirmed high susceptibility (S) of A. altissima to V. nonalfalfae but indicated tolerance (T) of Acer campestre, Acer pseudoplatanus and Quercus robur, possible resistance (PR) of Fraxinus excelsior, Populus nigra, Tilia cordata, Ulmus laevis and Ulmus minor and resistance (R) of Fraxinus pennsylvanica and Robinia pseudoacacia to this potential biocontrol agent. Results from seedling inoculations were confirmed by cursory field observations in Ailanthus-inoculated forest stands, where admixed A. campestre, A. pseudoplatanus, F. excelsior, Populus alba, R. pseudoacacia and U. laevis canopy trees remained asymptomatic, while mortality was induced in Ailanthus.     

Antifungal agents from heartwood extract of <Emphasis Type="Italic">Taiwania cryptomerioides</Emphasis> against brown root rot fungus <Emphasis Type="Italic">Phellinus noxius</Emphasis>

Taiwania (Taiwania cryptomerioides Hayata) is a native and plantation species in Taiwan, and its heartwood has demonstrated excellent decay resistance. Brown root rot fungus Phellinus noxius has caused severe damage to more than 100 tree species in Taiwan. The aims of this study were to investigate the antifungal activities of Taiwania heartwood extracts against P. noxius and to identify the antifungal compounds. Antifungal activities were examined using the agar dilution method (a direct contact assay) and the inverted lid method (a vapor contact assay). Active compounds were purified using liquid–liquid partition, open-column chromatography and HPLC. Among four soluble fractions (n-hexane, ethyl acetate, n-butanol and water soluble fractions), results showed that n-hexane soluble fraction (HSF) can significantly inhibit the growth of P. noxius via the agar dilution method. Moreover, active compounds present in HSF were obtained using antifungal assay-guided fractionation. Results showed that ferruginol, T-cadinol, α-cadinol and T-muurolol were found to exhibit excellent antifungal activities against P. noxius, and their IC₅₀ values were 16.9, 25.8, 33.8 and 50.6 μg/mL, respectively. According to the current findings, phytochemicals (ferruginol, T-cadinol, α-cadinol and T-muurolol) of Taiwania heartwood had the potential to be used as environmentally benign antifungal agents against P. noxius in place of synthetic or inorganic fungicides.     

Long-term growth performance of <Emphasis Type="Italic">Cordia africana</Emphasis> and <Emphasis Type="Italic">Grevillea robusta</Emphasis> trees in the Mount Kenya region

This study examined the long-term growth performance of Cordia africana and Grevillea robusta, which are the most common indigenous and exotic trees, respectively, associated with crops in the Mount Kenya region. Local farmers prefer G. robusta to C. africana as on-farm trees because they believe that G. robusta grows faster. Measurements of height and diameter at breast height were made of 47 C. africana and 89 G. robusta trees for which the age was established based on interviews with farmers. The oldest G. robusta and C. africana trees were 55 and 46 years old, respectively. The apical growth rate for G. robusta was greater than that for C. africana in Katheri (a humid area). The differences between the two species were less remarkable in Ruiri (a dry-subhumid area). There was no notable difference in the radial growth performance of the two species in Katheri and Ruiri. These comparisons suggest that the long-term growth performance of C. africana is not necessarily inferior to that of G. robusta.