Halys Egg Masses Research Articles

Field evaluation of symbiont-targeted control of Halyomorpha halys in hazelnut crop

Halyomorpha halys has emerged as one of the most damaging pests for hazelnut production. Due to the continuous reduction of available options for chemical control, alternative strategies are required. A promising and sustainable alternative is the use of symbiont-targeted control. Treatment of the egg surface with a biocomplex containing copper, zinc, and citric acid has been shown to effectively prevent the acquisition of the endosymbiont ‘Candidatus Pantoea carbekii’ by H. halys nymphs, resulting in high nymph mortality under laboratory conditions. The aim of this work was to assess the field efficacy of treatments targeting the H. halys symbiont in hazelnut orchards to optimize spray applications. Treatments with the anti-symbiont biocomplex were performed in an orchard infested with H. halys during 2022 and 2023. To assess product efficacy, H. halys egg masses were glued on cardboard tags and hung on different positions of plants canopy before the treatments. The wetting percentage of egg masses according to the position of the egg on the plant canopy was measured; eggs were then reared to evaluate nymphal mortality after hatching. Symbiont acquisition was measured by quantitative PCR. A preliminary test to set the spraying conditions revealed that a higher fan speed induced higher mortality of the newborns from treated egg masses, although it did not affect the wetting rate of cardboards. In addition, cardboard tags hung in the central part of the canopy and those closer to the sprayer showed the highest egg coverage, whereas those in the peripheral row were less covered. However, nymphal mortality was not correlated with the percentage of cardboard tags coverage, although it was correlated with symbiont acquisition. A significant reduction in the percentage of damaged hazelnuts was observed in the treated plot compared to an untreated control, confirming the efficacy of symbiont-targeted control in hazelnut orchards.

Age- and Density-Dependent Parasitism Rate and Development Time of the Generalist Egg-Parasitoid Ooencyrtus telenomicida (Hymenoptera: Encyrtidae) on Eggs of the Brown Marmorated Stink Bug, Halyomorpha halys.

Halyomorpha halys (Hemiptera: Pentatomidae) is an invasive pest species that was imported into Greece in 2011 and since then, has caused severe qualitative and quantitative damage to economically important crops. Its management relies mainly on the use of broad-spectrum insecticides, with little to no information available concerning the potential use of native parasitoids in terms of classical biological control. Our study aimed to assess the parasitism rate and development time of the gregarious egg parasitoid Ooencyrtus telenomicida (Hymenoptera: Encyrtidae) on H. halys egg-masses, depending on several factors such as: (i) age of parasitoids, (ii) density of parasitoids, (iii) age of host eggs, and (iv) oviposition experience of parasitoids. According to our results, the younger the host eggs and the more parasitoids, the higher the parasitism rate achieved by adults of O. telenomicida, with the maximum mean value of the parasitism rate observed with 1-day-old host eggs and 4 parasitoid pairs (57.3%). On the contrary, the lowest mean value of the parasitism rate was observed with 4-day-old host eggs and 1 parasitoid pair (6.5%). Similarly, the age of parasitoids significantly affected parasitisation. The older the parasitoids were, the higher the parasitism rate achieved by adults of O. telenomicida, with a three-fold higher parasitism rate observed at 3-4 and 5-6-day-old O. telenomicida, compared to 1-2-day-old (31.8, 32.4, and 12.1%, respectively). Individuals that developed in younger host eggs displayed a shorter development time, and the shortest development time was observed for O. telenomicida laid by 2 parasitoid pairs. Parasitoid age did not affect the development time of O. telenomicida, although there was a tendency for individuals laid by younger female parasitoids to exhibit a shorter development time. Our findings provide valuable information on the potential use of O. telenomicida as a biocontrol agent of H. halys.

Seasonal density and natural mortality of Halyomorpha halys (Stål) and indigenous stink bugs (Hemiptera: Pentatomidae) in a field crop agroecosystem.

Stink bugs (Hemiptera: Pentatomidae), including the exotic Halyomorpha halys (Stål), Nezara viridula (L.), and other indigenous species, are pests that damage a variety of agricultural crops. At a study site in the southeastern United States, we measured the density of stink bug species and patterns of parasitism and predation on corn, cotton, and soybean and host trees in an adjacent woodline. We assessed parasitism and predation of naturally laid egg masses in crops and sentinel egg masses in host trees and used pheromone-baited traps to determine H. halys seasonal development. Overall, H. halys and N. viridula were the dominant bugs observed. Adult H. halys were first detected each year on trees, followed by corn, and then cotton and soybean, suggesting that trees served as a source of H. halys dispersing into crops. For H. halys, more nymphs were captured in soybean than in corn or cotton. For N. viridula, more adults were captured in corn and cotton than in soybean, and more nymphs were captured in corn during 2019 and 2021 than in 2020. Percentage parasitism of N. viridula egg masses (74.2%) was higher than than that for H. halys egg masses (54.3%). Accordingly, conservation biological control has the potential to enhance parasitism of indigenous stink bugs and H. halys in field crop agroecosystems.

Habitat and vertical stratification affect capture of stink bugs (Hemiptera: Pentatomidae) and biological control of the invasive brown marmorated stink bug.

Spatiotemporal distribution of stink bugs (Hemiptera: Pentatomidae) and their natural enemies across farmscapes has been studied in more detail recently. However, the impact of plant height on vertical stratification of stink bugs and their natural enemies is rarely addressed across these diverse habitats. In this study, we examined capture of native stink bugs, the invasive brown marmorated stink bug, Halyomorpha halys (Stål)(Hemiptera:Pentatomidae), and a predaceous wasp, Astata occidentalis Cresson (Hymenoptera: Sphecidae) in pheromone-baited traps, in 2 habitats, woodlands of mostly deciduous trees mixed with some conifers and pecan orchards, in addition to their vertical stratification (0-13.7 m) at increasing heights. Furthermore, the effects of canopy height and habitat on H. halys egg mass predation and parasitism were evaluated. Adult H. halys were abundant in both habitats, but more nymphs were captured in pecan orchards. The same pattern was found for adult Euschistus servus (Say) (Hemiptera:Pentatomidae), Thyanta custator McAtee (Hemiptera:Pentatomidae), and A. occidentalis. In contrast, adult E. tristigmus (Say) (Hemiptera:Pentatomidae) and Chinavia hilaris (Say) (Hemiptera:Pentatomidae) were more abundant in woodlands. More nymphal H. halys and adults of E. servus, T. custator, and A. occidentalis were captured in ground traps than canopy traps in pecan. More adult and nymphal H. halys were captured at varying heights in the woodland canopy compared to near the ground as were adult E. tristigmus and C. hilaris. Both parasitism and predation occurred in woodland and pecan canopies. However, in one test we found that parasitism of H. halys egg masses occurred more often in the upper tree canopy, and more parasitism was detected in woodland than orchard habitat. In 2 tests, predation was higher in woodlands than pecan orchards. These results will aid in optimizing conservation biological control tactics in these habitats.

Releasing and tracking the distribution of adventive Trissolcus japonicus (Hymenoptera: Scelionidae) in Virginia.

Adventive populations of Trissolcus japonicus (Ashmead), an egg parasitoid of the invasive agricultural pest, brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), have been detected in the United States since 2014. Given its importance as an H. halys biocontrol agent, efforts to redistribute T. japonicus began within some US states. Our surveillance for T. japonicus in northwestern Virginia in 2016-2017 yielded annual detections only in 1 county. Thus, to promote its broader establishment, releases of H. halys egg masses parasitized by T. japonicus from Virginia occurred in 2018 (2 releases) and 2020 (1 release) at 9 sites throughout Virginia's tree fruit production regions. Monitoring of T. japonicus and H. halys, using yellow sticky cards deployed in H. halys host trees and pheromone-baited sticky traps, respectively, was conducted from 2018 to 2022. Annual captures of H. halys adults and nymphs appeared to reflect adequate populations to support T. japonicus establishment across most or all sites. Prerelease monitoring yielded a single T. japonicus at 1 site. By 2022, T. japonicus was detected at or near 7 of the remaining 8 release sites, with first detections varying between 1 and 2 yr from the releases in 2018 and 2020. Captures at most sites were very low, but establishment at several locations was indicated by detections in 2-4 seasons. In 2022, T. japonicus surveillance at 11 additional sites in northwestern Virginia yielded detections at all locations, including those at which it had not been detected in 2016-2017, providing evidence for its range expansion.

Predation and parasitism of naturally occurring and sentinel stink bug egg masses ofHalyomorpha halys(Stål) andNezara viridula(L.) (Hemiptera: Pentatomidae) in various southeastern habitats

Stink bugs, including Halyomorpha halys (Stål) and Nezara viridula (L.), are agricultural pests that feed on fruit in a variety of crops. Monitoring predation and parasitism of stink bug egg masses furthers our understanding of potential biological control tactics. However, best practices for laboratory and field assessments of parasitism and predation of egg masses require further attention. We carried out a series of laboratory and field experiments to test whether parasitism and predation for three types of sentinel H. halys egg masses, fresh, frozen, and refrigerated, varied in agricultural commodities. In addition, we asked if predation and parasitism differed between sentinel and naturally occurring H. halys and N. viridula egg masses in soybean. In the laboratory, more H. halys eggs were parasitized by Trissolcus euschisti (Ashmead) (Hymenoptera: Scelionidae) if they were frozen or refrigerated compared to fresh eggs. Similarly, in the field, parasitism was higher for frozen egg masses than fresh. In 2018 and 2019, H. halys natural egg masses had higher parasitism and lower predation compared to sentinel egg masses in soybean. In a paired field test during 2020 and 2021, there was no difference in parasitism between H. halys natural and sentinel eggs, but much higher incidence of parasitism was detected in natural N. viridula egg masses than sentinel eggs. Collecting natural egg masses is the best methodology for field assessment of parasitism of stink bug egg masses; however, if natural egg masses are not easily available, deploying refrigerated sentinel egg masses is a good alternative.

Efficacy of Kairomone Lures to Attract Parasitoids of Halyomorpha halys

In its native range, Halyomorpha halys (Stål) is suppressed by parasitoids in the genus Trissolcus (Hymenoptera: Scelionidae). Trissolcus native to Utah have demonstrated low parasitism of H. halys, while adventive Trissolcus japonicus (Ashmead) have shown parasitism of up to 20%. Custom rubber septa lures containing stink bug kairomones, n-tridecane (attractant), and (E)-2-decenal (repellent), at 100%, 90%, and 80% levels of attractant (10 mg load rate), were placed adjacent to sentinel H. halys egg masses in northern Utah field trials. Egg masses were evaluated for the presence and intensity (proportion of parasitized eggs) of parasitism. Parasitism by T. japonicus and T. euschisti (Ashmead) was low; however, the 100% lure showed double the parasitism of the control and more than three times that of the 90% and 80%. Two-way choice mesocosm trials in the laboratory evaluated previous lures and a lower load rate of 5 mg-100% attractant treatment. Lures of 10 mg at 100% and 80% were more attractive to T. japonicus than the control, while 5 mg at 100% and 10 mg at 90% showed no significant attraction. Our results support a proof-of-concept of rubber septa as release devices for kairomones to attract T. japonicus and provide a baseline for future field-based studies.

Adventive Population ofTrissolcus japonicus(Hymenoptera: Scelionidae), Parasitoid ofHalyomorpha halys(Hemiptera: Pentatomidae), Discovered in Southwestern Idaho

AbstractAdventive populations of Trissolcus japonicus (Ashmead) have been detected in the eastern and western United States including the western states of Washington, Oregon, California, and Utah. These populations may provide classical biological control for the invasive brown marmorated stink bug, Halyomorpha halys (Stål), which can cause economic loss to many specialty crops in western North America. Idaho has not previously been surveyed for the exotic T. japonicus or native parasitoids of H. halys. In July 2021, T. japonicus was discovered emerging from wild H. halys egg masses in Star, Idaho (43.69788, −116.49427), and was detected on yellow sticky cards from July to September. This is the first record of T. japonicus in the state of Idaho. T. japonicus constituted only a small portion of Trissolcus species detected; other species included T. euschisti (Ashmead), T. hullensis (Harrington), and T. utahensis (Ashmead). Genetic population level analysis of T. japonicus specimens from Idaho supports the likelihood of its expansion inland from the west coast, inhabiting ecozones previously considered unsuitable due to high temperatures and low humidity. This report opens the prospect of an effective biological control agent for H. halys in Idaho and potentially other hot and dry geographic regions and expands documentation of the presence of adventive T. japonicus populations in North America.

No adverse effects of symbiotic control on the parasitism of Halyomorpha halys by egg parasitoids

The brown marmorated stink bug Halyomorpha halys is a polyphagous insect, which has a devastating impact on agricultural production in many countries. The alteration of symbiont vertical transmission, by removing symbionts from stink bug eggs (symbiotic control), has been recently introduced in control programmes against this insect. A major advantage of this strategy is the compatibility with natural enemies, since it allows an insecticide-free approach that is not harmful to other agroecosystem components. However, the effect of anti-symbiont products on parasitism by egg parasitoids is still unexplored. Here, we investigated the impact on parasitism by native (Anastatus bifasciatus, Ooencyrtus telenomicida and Trissolcus kozlovi) and exotic (Trissolcus japonicus and Trissolcus mitsukurii) parasitoids that attack H. halys eggs, after treatment with the micronutrient biocomplex Dentamet®, used for symbiotic control. The native wasp species were tested in no-choice bioassays, showing that treatment of the egg masses did not affect emergence percentages, but the non-reproductive effects were often reduced by the biocomplex. The exotic species T. japonicus and T. mitsukurii were used in no-choice and paired choice bioassays, showing an opposite influence of Dentamet® on emergence percentage and preference in the two species. No-choice tests indicated the highest successful parasitoid emergence on biocomplex-treated egg masses for T. japonicus, while no preference in the paired comparison with eggs treated with water or untreated. In contrast, T. mitsukurii displayed the lowest parasitism after Dentamet® treatment in no-choice tests, and preferred egg masses without Dentamet® in paired choice tests. We did not record any natural symbiont acquisition by the parasitoids emerged from H. halys egg masses, indicating that the wasp fitness is very unlikely to be altered by dysbiotic effects resulting from treatments. Therefore, our results support a further implementation of symbiotic control in different crops in combination with biological control, as sustainable options for H. halys integrated pest management.

Interspecific competition between Trissolcus japonicus and Trissolcus mitsukurii, two promising candidates for biocontrol of Halyomorpha halys

The invasive stink bug Halyomorpha halys, native to east Asia, is a severe agricultural pest of worldwide importance and biocontrol is a promising method for its long-term management. The two Asian egg parasitoids Trissolcus japonicus and Trissolcus mitsukurii are considered to be effective candidates as biological control agents. These species can co-occur in the same habitats and interspecific competition for hosts could therefore have an important role in natural control. We assessed the foraging behavior and the progeny production of both species under laboratory conditions with three different interspecific competition scenarios. With indirect competition, H. halys egg masses previously parasitized by the female of one species were offered to the competitor females after 0, 3, 5, or 7 days. With direct extrinsic competition, females of each species were tested in arenas either when introduced simultaneously (synchronous release) or when half of the host egg mass had already been parasitized by the other species (asynchronous release). Both Trissolcus species were able to parasitize host eggs already parasitized by the other species, although the progeny production always favored the species that arrived first on the host egg mass. However, in the synchronous releases scenario, T. mitsukurii displayed more aggressive behavior and spent more time defending the host egg mass than T. japonicus, resulting in a higher progeny production. Our results showed that multiparasitism among T. japonicus and T. mitsukurii, at least under laboratory conditions, resulted in a general waste of searching time, energy, eggs laid, and a lower reproductive potential by the second-arriving species on the host egg mass.

Evaluating Chemical Cues Associated with Halyomorpha halys Toward Enhanced Sensitivity of Surveillance for Trissolcus japonicus.

In Asia, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is the predominant egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). Detections of adventive T. japonicus populations in North America since 2014, where invasive H. halys populations have impacted various specialty crops, spurred surveillance efforts to track T. japonicus, and yellow sticky cards (YSC) deployed in H. halys host trees have proven effective for this purpose. While T. japonicus exhibits positive behavioral responses to several olfactory stimuli associated with H. halys under laboratory conditions, these have not been evaluated for their potential utility to enhance surveillance of T. japonicus in the field. In northwestern Virginia, where both H. halys and T. japonicus are well-established, we examined the effect of baiting tree of heaven, Ailanthus altissima (Mill.) Swingle (Sapindales: Simaroubaceae), with lures containing the H. halys aggregation pheromone and pheromone synergist on the abundance of H. halys egg masses and captures of T. japonicus in YSC. We also assessed the effect of baiting YSC with newly-laid H. halys egg masses or n-tridecane, a component of H. halys tarsal prints, on T. japonicus captures. Destructive sampling of pheromone-baited and nonbaited trees revealed no significant differences in H. halys egg mass abundance on foliage. Similarly, YSC deployed in pheromone-baited and nonbaited trees showed no significant differences in T. japonicus captures. Moreover, YSC augmented with H. halys egg masses or n-tridecane showed no increase in T. japonicus captures compared with nonbaited controls. The implications for surveillance of adventive T. japonicus are discussed.

Augmentative biological control of Halyomorpha halys using the native European parasitoid Anastatus bifasciatus: Efficacy and ecological impact

We report the first large-scale augmentative biological control project carried out in Europe against Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) using the native egg parasitoid Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae). During summer 2020, a total of 325,000 adults of A. bifasciatus were released at a rate of 1000 individuals/ha of orchard in 11 sites in Trentino-Alto Adige (Northern Italy). Parasitism parameters were compared between release and control (no release) sites, in which at least three egg masses naturally laid by H. halys were collected (for a total of 262 egg masses). Anastatus bifasciatus and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) were the dominant parasitoids, but parasitism by both species fluctuated widely among sites. At release sites, A. bifasciatus showed a significantly higher discovery efficiency (31.4%) and parasitism rate (16.7%) of H. halys egg masses than at control sites (1.7% and 1.2%, respectively). Parasitism by A. bifasciatus was not dependent on egg mass abundance at release sites, but at control sites a host density-dependent response was revealed by a positive relationship between parasitism and number of H. halys egg masses. On the other hand, parasitism by the adventive T. mitsukurii was not affected by either the releases of A. bifasciatus or by the abundance of H. halys egg masses per site. In conclusion, augmentative releases of A. bifasciatus contributed to increasing its parasitization of H. halys, without causing any negative effects on parasitization by naturally occurring species.

Influence of Trap Location in the Tree Canopy on Captures of Adventive Trissolcus japonicus (Hymenoptera: Scelionidae)

Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is an egg parasitoid of the invasive Asian pest, brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). Also native to Asia, adventive T. japonicus populations have been detected in North America since 2014, and are currently reported from 15 U.S. states, the District of Columbia, and two Canadian provinces. Yellow sticky cards (YSC) have proven effective for monitoring the presence, seasonal abundance, and distribution of these adventive populations. Our research has utilized YSC deployed in the midcanopy of H. halys host trees, following a study in which all leaves on felled tree of heaven, Ailanthus altissima (Mill.) Swingle, were inspected for H. halys egg masses, yielding eggs parasitized by T. japonicus only from mid- and upper-canopy leaves. However, given that other investigators have captured T. japonicus using YSC deployed in the lower-canopy, and that the effect of YSC placement in trees on T. japonicus captures had not been examined, captures of T. japonicus on YSC in the mid- and lower-canopy of individual A. altissima were compared. Traps were replaced weekly for five weeks and assessed for scelionid species. In 2020 and 2021, T. japonicus represented ≥53% of all Scelionidae captured, and there was not a significant effect of YSC location in the canopy on its captures. Deploying YSC at either canopy height was effective for measuring the relative abundance of T. japonicus, but sampling from the lower canopy substantially improved the efficiency and convenience of T. japonicus surveillance.

Semi-natural habitats promote biological control of Halyomorpha halys (Stål) by the egg parasitoid Trissolcus mitsukurii (Ashmead)

The invasive alien species Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a major pest of kiwifruit and other fruit crops. Adventive populations of the Asian egg parasitoid Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) were found in the north of Italy in 2016. Halyomorpha halys abundance was monitored in 14 kiwifruit orchards located in north-eastern Italy, and H. halys egg masses were sampled within kiwifruit orchards to assess the impact of egg parasitoids. Both H. halys populations and parasitoid impacts were evaluated considering the influence of ecological structures, and in particular the distance from semi-natural habitats constituted by riparian vegetation buffers and the presence of hedgerows surrounding the orchard. Halyomorpha halys populations fluctuated during the two seasons surveyed, and adults were more abundant during the first year of the study. In addition, more adults were detected in kiwifruit orchards located close to the riparian vegetation and decreased along with the distance from this habitat. Trissolcus mitsukurii had higher parasitism rates on H. halys eggs than the native Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae). No effect of hedgerows was observed on parasitoid impacts in orchards, while a relationship was detected with distance from riparian vegetation: a high T. mitsukurii parasitism rate was observed in kiwifruit orchards close to riparian vegetation buffers. Our findings demonstrate that semi-natural habitats constituted by large patches of unmanaged vegetation promote biological control of H. halys by the introduced egg parasitoids.

First Report of Native Parasitoids of Halyomorpha halys (Hemiptera: Pentatomidae) in Greece.

Simple SummaryThe brown marmorated stink bug (BMSB) is a polyphagous species that causes severe damage to tree fruit, small fruit, vegetables, ornamental crops, and field crops. Classical biological control is one potential long-term and low-cost strategy to control the BMSB, using natural enemies. However, no natural enemy native to Greece that infects BMSB has been reported yet. Herein, we report the occurrence of two native hymenopteran egg parasitoids—Anastatus bifasciatus and Ooencyrtus telenomicida. Both egg parasitoids were collected from egg masses of the BMSB in the region of Thessaloniki, northern Greece. The total parasitism rate was 8.5%. Furthermore, A. bifasciatus was collected in mid-June and mid-August on egg masses of BMSB that were laid on green beans, apricots, and olives. On the other hand, O. telenomicida was only collected in mid-June, on one egg mass of BMSB that was laid on apricots. This first record could actually facilitate, for future tasks, the biological control of H. halys in Greece.Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an endemic species of East Asia; it was introduced into Europe in 2007. It has a wide range of hosts as it feeds on over 170 host plant species and significantly impacts crop production. In Greece, H. halys causes significant losses in the production of kiwi, peaches, and green beans; thus, control of this species (including biological control) is essential. Here, we focus on the potential impact of native natural enemies of H. halys in Greece. From June to October 2020, we sampled naturally field-laid H. halys egg masses to recover native parasitoids. A total of 20 egg masses of H. halys were collected from infested fields from different locations in northern Greece. Out of 529 eggs, 45 parasitoids managed to hatch successfully. The overall parasitism rate was 8.5%. We found two species of Hymenopteran egg parasitoids attacking H. halys eggs—Anastatus bifasciatus (Geoffrey) (Hymenoptera: Eupelmidae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), with the former comprising 58% of all parasitoids that were recovered. These results contribute to the knowledge about the natural enemy community that attacks H. halys in Greece, and the use of these native egg parasitoids in biological control programs may be a viable H. halys management strategy.

Hyperparasitism of Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) on Two Biological Control Agents of Halyomorpha halys.

Simple SummaryThe brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive pest that causes losses to many crops in different parts of the world. Biological control programs using the egg parasitoids Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) have been proposed as sustainable strategies to control this pest. Acroclisoides sinicus (Huang and Liao) is another parasitoid that frequently emerged from H. halys egg masses, hypothesized to be a hyperparasitoid of Trissolcus spp. that can have a potentially negative effect on the outcome of biological control programs. Under laboratory conditions, we investigated the impact of A. sinicus on the two primary parasitoids of H. halys, assessing its host preference and exploitation capacity. Acroclisoides sinicus demonstrated a clear preference in parasitizing T. mitsukurii, while the impact on T. japonicus was relatively low. Acroclisoides sinicus can use volatiles emitted by egg masses to distinguish between those parasitized by T. mitsukurii from those parasitized by T. japonicus or unparasitized ones. The results obtained here suggest that the presence of the hyperparasitoid can affect the composition of H. halys parasitoid complex.Halyomorpha halys (Stål) is an invasive Asian pest that causes severe crop losses on various crops. Nowadays, management strategies against this pest mainly rely on pesticide use, but biological control with egg parasitoids is considered the most promising long-term and sustainable solution. Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) are Asian egg parasitoids already present in Europe and are the most effective biological control agents of H. halys. Therefore, these two species are considered for biological control programs in Europe and other parts of the world. Acroclisoides sinicus (Huang and Liao) is a pteromalid parasitoid wasp that frequently emerged from H. halys egg masses collected in northern Italy. This species has been hypothesized to be a hyperparasitoid of Trissolcus spp. parasitoids. This study was carried out under laboratory conditions where A. sinicus was tested in no-choice and two-choice experiments to assess the host preference between T. japonicus and T. mitsukurii. Olfactory responses of A. sinicus from volatiles emitted from different potential hosts were also tested. In all trials, A. sinicus showed a clear preference for parasitizing H. halys eggs previously parasitized by T. mitsukurii compared to T. japonicus. In no-choice experiments, the impact of the hyperparasitoid on T. japonicus was low, showing an exploitation rate of 4.0%, while up to a 96.2% exploitation rate was observed on T. mitsukurii. Acroclisoides sinicus was also attracted by volatiles emitted by egg masses parasitized by T. mitsukurii, while no response was observed to egg masses parasitized by T. japonicus or not parasitized. Therefore, according to the results obtained here, A. sinicus could limit the population development of T. mitsukurii, while lesser effects are expected on T. japonicus.

Add Germany to the List-Adventive Population of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) Emerges in Germany.

Simple SummaryThe brown marmorated stink bug, Halyomorpha halys, is an invasive pest species of global economic importance. It has a very broad host range and causes severe damages in agricultural, horticultural, and fruit crops. Control measures, including available chemical and mechanical options, have often proved insufficient. Surveys of natural enemies in the newly invaded areas have also shown that natural biological control is generally too low to control H. halys populations in the long run. In its native Asian range, egg parasitoids in the genus Trissolcus play an important role in controlling H. halys. Since the mid-2010s, adventive populations of Trissolcus japonicus, a dominant egg parasitoid of H. halys in Asia with a narrow host range, have been reported from several countries with prior establishment of H. halys. Here, we report the first discovery of T. japonicus in Germany. This finding corroborates a northbound expansion of the range of T. japonicus in Europe, along with H. halys.The brown marmorated stink bug, Halyomorpha halys, is a polyphagous pest species of worldwide economic importance. Since the mid-1990s, it has invaded and become established in various countries outside its native Asian range. In the newly invaded areas, biological control by native natural enemies has been shown to be insufficient in the long-term control of this severe pest. Adventive populations of Trissolcus japonicus, an important biological control agent of H. halys in Asia, have been reported from North America and some European countries since the mid-2010s. This egg parasitoid species seems to follow in the wake of the establishment of H. halys populations outside their native Asian range. Here, we report the first discovery of an adventive population of T. japonicus in Germany. In 2020, adult T. japonicus were recovered from parasitized H. halys egg masses (naturally laid and sentinel egg masses) and collected in ruderal areas using an insect suction sampler. The arrival of T. japonicus in Germany, unintentional through pathways yet unknown, corroborates a northbound expansion of its range within Europe. Further field surveys will show the extent of its dispersal and establishment capacities within this new distribution area.

An Effective Cold Storage Method for Stockpiling Halyomorpha halys (Hemiptera: Pentatomidae) Eggs for Field Surveys and Laboratory Rearing of Trissolcus japonicus (Hymenoptera: Scelionidae).

An effective stockpiling method for egg masses of the invasive brown marmorated stink bug (Halyomorpha halys [Stål]; Hemiptera: Pentatomidae) would be useful for rearing and field studies of its egg parasitoid Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae). The current method of stockpiling H. halys egg masses at subzero temperatures has lethal and sublethal fitness consequences for T. japonicus. Our goal was to test the efficacy of refrigeration as an alternative method for stockpiling H. halys eggs. We show that parasitoid emergence from egg masses refrigerated at 8°C for up to two months before parasitism is higher than from frozen egg masses. In addition, 8°C cold storage usually had minimal or no sublethal fitness effects on emerging T. japonicus. Only after two months of host egg refrigeration did the emergence of T. japonicus begin to decrease significantly (by ~10% relative to untreated viable egg masses), whereas egg masses previously frozen at -80°C had a ~59% reduction in parasitoid emergence after 14 d of storage. Refrigerated egg masses that were subsequently exposed to a range of field-realistic average temperatures were still suitable for T. japonicus parasitism after 7 d. Our results demonstrate that refrigeration at 8°C, while resulting in complete mortality of H. halys embryos after 10 d, are more suitable for T. japonicus parasitism than those stored at -80°C. The quantity and quality of H. halys eggs that can be stockpiled with this method could facilitate T. japonicus laboratory colony maintenance, field monitoring, and releases.

Optimization of Trissolcus japonicus cold storage methods for biological control of Halyomorpha halys

Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) has shown promise as a biological control agent for the invasive agricultural and nuisance pest, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). In addition to the need for laboratory research colonies, the possibility for rearing T. japonicus for classical or augmentative releases necessitates investigation into efficient rearing protocols with control over timing of production. Cold storage is a means to slow insects’ metabolism and cold temperatures can be used to manipulate when and how many parasitoids are available for use. Conditions of cold storage (i.e., temperature and photoperiod), duration of exposure to cold, nutrition, age, and sex of parasitoids can all affect the success of a cold storage regime. We tested how these factors affected mortality, realized fertility of females, sex of progeny, and development time for cold-stored adult and immature T. japonicus using previously frozen H. halys egg masses. Rearing adult T. japonicus at 8, 13, or 18 °C (10:14 h L:D) significantly increased longevity compared to 23 °C (16:8 h L:D); however, for females reared at 8 °C, 10:14 h L:D, we found sublethal effects on realized fertility and sex of their progeny. Adults with access to food survived at greater levels than those without food. We found high mortality of cold-stored immatures in all the ages and cold storage conditions tested. Additionally, differences in T. japonicus emergence from fresh and frozen H. halys eggs was assessed. This work can be used to compare the costs and benefits of cold storage for T. japonicus and will assist forecasting the emergence and sex of adult parasitoids after T. japonicus are cold stored.

Rearing Trissolcus japonicus and Trissolcus mitsukurii for Biological Control of Halyomorpha halys.

Simple SummaryHalyomorpha halys is a severe agricultural pest of Asian origin, which threatens cultivation of vegetables and fruits worldwide. Classical biological control is foreseen as the most effective approach to reduce populations of H. halys. The egg parasitoid Trissolcus japonicus is the most important candidate biological control agent. Adventive populations of T. japonicus are already present in limited distributions in North America and in Europe. Trissolcus mitsukurii is a second Asian species that attacks H. halys and has been found in Northern Italy. Efficient laboratory rearing procedures of these biological control agents are needed for release programs to help control the pest. We present data that will help to optimize progeny production with minimal effort.Halyomorpha halys is a severe agricultural pest of Asian origin that has invaded many countries throughout the world. Pesticides are currently the favored control methods, but as a consequence of their frequent use, often disrupt Integrated Pest Management. Biological control with egg parasitoids is seen as the most promising control method over the long-term. Knowledge of the reproductive biology under laboratory conditions of the most effective candidates (Trissolcus japonicus and Trissolcus mitsukurii) for optimizing production for field releases is strongly needed. Rearing of these egg parasitoids was tested by offering three different host supply regimes using new emerged females and aged, host-deprived females in different combinations. Results showed a mean progeny per female ranging from 80 to 85 specimens for T. japonicus and from 63 to 83 for T. mitsukurii. Sex ratios were strongly female biased in all combinations and emergence rates exceeded 94% overall. Cumulative curves showed that longer parasitization periods beyond 10–14 days (under the adopted rearing regimes) will not lead to a significantly increase in progeny production. However, ageing females accumulate eggs in their ovaries that can be quickly laid if a sufficient number of host eggs are supplied, thus optimizing host resources. Our data showed that offering H. halys egg masses to host-deprived female Trissolcus once a week for three weeks allowed its eggs to accumulate in the ovary, providing the greatest number of offspring within a three week span.