Halys Eggs Research Articles

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.

Native and Non-Native Egg Parasitoids Associated with Brown Marmorated Stink Bug (Halyomorpha halys [Stål, 1855]; Hemiptera: Pentatomidae) in Western Slovenia.

Simple SummaryHalyomorpha halys, the brown marmorated stink bug (BMSB), is an invasive pest causing serious damage to agricultural production. Managing this pest species is challenging because of its wide host range and lack of effective control measures. Biological control of H. halys through natural enemies seems to be the most environmentally friendly and sustainable solution. Extensive knowledge of the native egg parasitoid fauna is needed prior to the introduction of a biological control program. The main purpose of the study, carried out in the Goriška region of Western Slovenia, was to detect egg parasitoid species associated with H. halys and to evaluate their impact on the pest population under local environmental conditions. High species richness was identified during the study, and five egg-parasitoids were recorded for the first time in Slovenia. The native species Anastatus bifasciatus dominated in urban and suburban areas, while the non-native Trissolcus mitsukurii prevailed in agricultural areas. Rapid recruitment of native parasitoids, the presence of an effective alien parasitoid species in the region and increasing overall parasitism rates are very encouraging results and valuable information for future activities regarding the biological control of H. halys in Slovenia.Halyomorpha halys (Hemiptera: Pentatomidae), native to East Asia, has become a globally invasive pest, as a serious threat to agricultural production and a notorious nuisance pest in urban areas. Considerable efforts have been made so far to develop effective pest control measures to prevent crop damage. Biological control of this invasive stink bug by egg parasitoids has proven to be the most environmentally sustainable long-term solution. Knowledge of the native egg parasitoid fauna is of key importance when implementing a biological control program. Therefore, the main objective of our study was to detect egg parasitoid species associated with H. halys in the Goriška region (Western Slovenia) and to evaluate their impact on the pest population under field conditions. In the years 2019 and 2020, around 4600 H. halys eggs were collected in the wild and more than 3400 sentinel eggs were exposed to detect parasitoids in the field. Five egg-parasitoid species emerged from H. halys eggs: Anastatus bifasciatus (Hymenoptera: Eupelmidae), Telenomus sp., Trissolcus basalis, Trissolcus mitsukurii (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Hymenoptera: Encyrtidae), all of them are new records for Slovenia. The native species, An. bifasciatus, dominated in urban and suburban areas, while non-native Tr. mitsukurii prevailed in agricultural areas. Overall parasitism rates of naturally laid eggs by the parasitoid species complex in 2019 and 2020 was 3.0 and 14.4%, respectively. Rapid recruitment of native parasitoids, early detection of an effective alien parasitoid species and increasing overall parasitism rates are very encouraging results, which need to be followed and verified in future research.

Trissolcus kozlovi in North Italy: Host Specificity and Augmentative Releases against Halyomorpha halys in Hazelnut Orchards

Simple SummaryThe Asian brown marmorated stink bug, Halyomorpha halys, is an invasive crop pest introduced into Europe in the 2000s. Due to its high harmfulness, and the increased chemical use for its control in the invaded areas, research has focused on biological control. In North Italy, the native parasitoid Trissolcus kozlovi emerged from field-collected H. halys eggs and proved to successfully parasitize H. halys eggs in the laboratory. Therefore, since little is known on T. kozlovi, this study aimed at assessing its physiological host range on 12 bug species in the laboratory, as well as its potential as a biological control agent of H. halys in the field by releases in two hazelnut orchards. In the laboratory, among the tested bug species, only Nezara viridula was an unsuitable host. On all others, T. kozlovi was able to develop, even if at different levels, suggesting that it is as oligophagous as Trissolcus japonicus, with which it shares many similarities. In the field, T. kozlovi was found to parasitize H. halys eggs, but only immediately after field releases. Therefore, further field surveys are required to assess its favorably environmental conditions and its possible interaction with T. japonicus, currently present in Italy.Trissolcus kozlovi (Hymenoptera: Scelionidae) emerged from field-laid eggs of Halyomorpha halys (Hemiptera: Pentatomidae) in North Italy, and it emerged in significantly higher numbers from fresh H. halys eggs compared to other native scelionids. Since few data on T. kozlovi are available, its host-specificity and some biological traits were investigated in laboratory tests, and its impact after augmentative releases was evaluated in two hazelnut orchards. Among the 12 tested bug species (Hemiptera: Pentatomidae, Scutelleridae), only Nezara viridula was an unsuitable host, while the highest offspring proportions were obtained from Arma custos, Pentatoma rufipes, and Peribalus strictus, followed by Acrosternum heegeri and Palomena prasina. Furthermore, when reared on P. strictus, T. kozlovi showed a high longevity as well as a high adaptation to H. halys eggs. In both hazelnut orchards, T. kozlovi emerged from H. halys eggs after field releases, but it was not found in the next two years. The physiological host range of T. kozlovi was quite similar to that of T. japonicus, and probably T. kozlovi has just begun to attack H. halys as a new host. This aspect needs to be further investigated, as well as its favorable environmental conditions, its distribution and also its possible interaction with T. japonicus, currently present in Italy.

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.

Assessing the Distribution of Exotic Egg Parasitoids of Halyomorpha halys in Europe with a Large-Scale Monitoring Program.

Simple SummaryThe management of invasive alien species is a very challenging task. For the brown marmorated stink bug (Halyomorpha halys), classical biological control has been identified as the most suitable method to sustainably reduce its populations in the long-term. Among its natural enemies, two species were identified as the most promising candidates for biocontrol, Trissolcus japonicus and Trissolcus mitsukurii. Populations of these two species have recently been detected in Europe and to assess their distribution, a large-scale study was performed. Combining several monitoring methods, in four months (May–September 2019), a wide area covering northern Italy and parts of Switzerland was surveyed. The results showed that both species have spread into all types of habitats where H. halys is present and the parasitization of native species was rarely observed. Among native species, Anastatus bifasciatus was the predominant parasitoid of H. halys. This study supported the development of the first release program of Tr. japonicus in Europe.The brown marmorated stink bug Halyomorpha halys is an invasive agricultural pest with a worldwide distribution. Classical biological control has been identified as the most promising method to reduce the populations of H. halys. Adventive populations of two candidates for releases, Trissolcus japonicus and Trissolcus mitsukurii, have recently been detected in Europe. To assess their distribution and abundance, a large-scale survey was performed. From May to September 2019, a wide area covering northern Italy and parts of Switzerland was surveyed, highlighting the expanding distribution of both Tr. japonicus and Tr. mitsukurii. Within four years after their first detection in Europe, both species have rapidly spread into all types of habitats where H. halys is present, showing a wide distribution and continuous expansion. Both exotic Trissolcus showed high levels of parasitism rate towards H. halys, while parasitization of non-target species was a rare event. The generalist Anastatus bifasciatus was the predominant native parasitoid of H. halys, while the emergence of native scelionids from H. halys eggs was rarely observed. The presence of the hyperparasitoid Acroclisoides sinicus was also recorded. This study provided fundamental data that supported the development of the first inoculative release program of Tr. japonicus in Europe.

Predation of the brown marmorated stink bug, Halyomorpha halys by the Japanese acrobat ants, Crematogaster matsumurai and Crematogaster osakensis

Halyomorpha halys (Hemiptera: Pentatomidae) is an invasive pest native to Asia that causes severe economic losses in agriculture around the world. Although chemical control is relied upon for control of this pest, better long-term solutions are needed to achieve sustainable control. Currently, information is scarce on the complex of predators regulating populations of H. halys in its native region. Through laboratory bio-assays, we investigated the predatory ability of two species of acrobat ant native to Japan, Crematogaster matsumurai and C. osakensis, and the invasive Argentine ant, Linepithema humile, presented with different immature life stages of H. halys. Results indicated that these Japanese Crematogaster ants did not prey on the H. halys eggs or affect their eclosion, but did reduce the survival of early (first, second, and third) instar nymphs. Crematogaster matsumurai limited the survival of first, second, and third instar nymphs to 0%, 40%, and 73% respectively, and C. osakensis reduced their survival to 0%, 13%, and 60%, respectively. Predation of immature H. halys by L. humile reduced the survival of all instars to zero under the laboratory conditions. These data suggest that generalist Japanese Crematogaster ants may play an important role in reducing immature survival of H. halys in their native range, but likely act additively with other natural enemies that inflict mortality on different life stages. This work demonstrates that ants deserve consideration in the development of integrated pest management strategies for H. halys.

Influence of Holding Conditions and Storage Duration ofHalyomorpha halys(Hemiptera: Pentatomidae) Eggs on Adventive and Quarantine Populations ofTrissolcus japonicus(Hymenoptera: Scelionidae) Behavior and Parasitism Success

Halyomorpha halys (Stål) is an invasive pest in the United States and other countries. In its native range, H. halys eggs are parasitized by a co-evolved parasitoid, Trissolcus japonicus (Ashmead). In the United States, T. japonicus, a classical biological control candidate, is being redistributed in many states where adventive populations exist. To establish if H. halys egg holding conditions affect T. japonicus foraging behavior or successful parasitism, naïve, female parasitoids from an adventive population were allowed to forage in laboratory bioassay arenas with either fresh or frozen (-20 or -80°C) egg masses, the latter held for five durations ranging from 1 h to 112 d. Parasitoid movements were recorded for 1 h. Thereafter, parasitoids were transferred with the same egg mass for 23 h. Additionally, female parasitoids from a quarantine colony were exposed to: 1) pairs of fresh egg masses and egg masses frozen at -40°C (>24 h) or 2) a single fresh egg mass or egg mass frozen at -40°C (<1 h). All exposed egg masses were held to assess progeny emergence. In the foraging bioassay, holding temperature and storage duration appeared to influence host-finding and host quality. Egg masses held at -80°C and fresh egg masses resulted in significantly greater levels of parasitism and progeny emergence compared with eggs held at -20°C. No differences were recorded between egg masses held at -40°C for ≤1 h and fresh egg masses. These results will help refine methods for preparation of egg masses for sentinel monitoring and parasitoid mass rearing protocols.

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.

Temperature and Humidity Interact to Influence Brown Marmorated Stink Bug (Hemiptera: Pentatomidae), Survival.

High-temperature events can influence insect population dynamics and could be especially important for predicting the potential spread and establishment of invasive insects. The interaction between temperature and environmental humidity on insect populations is not well understood but can be a key factor that determines habitat range and population size. The brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive agricultural pest in the United States and Europe, which causes serious economic damage to a wide range of crops. This insect's range continues to expand. It has recently invaded the Central Valley of California, which has a hotter and drier climate compared with the Eastern United States where this insect is established. We investigated how high-temperature events and relative humidity would impact the survival and reproduction of H. halys. Using incubators and humidity chambers, we evaluated the impact of humidity and short-term (2 d) high-temperature exposure on the survival and development of H. halys eggs, nymphs, and adults. We found that high temperatures significantly reduced H. halys survival. The impact of humidity on H. halys survival was dependent on temperature and life stage. Low humidity decreased first-instar survival but not third- to fourth-instar survival. High humidity increased first instar survival but decreased third- to fourth-instar survival. Humidity did not influence adult or egg survival. We also found that high temperatures decreased H. halys reproduction. Our findings have important implications for understanding the invasive ecology of H. halys and may be used to improve models predicting H. halys range expansion.

Hidden Host Mortality from an Introduced Parasitoid: Conventional and Molecular Evaluation of Non-Target Risk.

Hidden trophic interactions are important in understanding food web ecology and evaluating the ecological risks and benefits associated with the introduction of exotic natural enemies in classical biological control programs. Although non-target risk is typically evaluated based on evidence of successful parasitism, parasitoid-induced host mortality not resulting in visible evidence of parasitism (i.e., nonreproductive effects) is often overlooked. The adventive establishment of Trissolcus japonicus, an exotic parasitoid of the introduced stink bug Halyomorpha halys, provides an opportunity to investigate the total impact of this parasitoid on target and non-target hosts in the field. We developed a new methodology to measure nonreproductive effects in this system, involving a species-specific diagnostic PCR assay for T. japonicus. We applied this methodology to field-deployed eggs of four pentatomid species, coupled with traditional rearing techniques. Nonreproductive effects were responsible for the mortality of an additional 5.6% of H. halys eggs due to T. japonicus, and were even more substantial in some of the non-target species (5.4-43.2%). The observed hidden mortality of native non-target species from an introduced parasitoid could change predictions about direct and indirect ecological interactions and the efficacy of biological control of the target pest.

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.

Fitness and interspecific competition of Trissolcus japonicus and Anastatus japonicus, egg parasitoids of Halyomorpha halys

Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) and Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae) are the most important egg parasitoids of Halyomorpha halys Stål (Hemiptera: Pentatomidae) in northern China. In this study, we assessed the fitness of these two parasitoid species at different temperatures. We examined the intrinsic competition of these parasitoids inside host eggs by providing each parasitoid species with H. halys egg masses previously parasitized by the other species, at different time intervals between attacks. We also investigated their intraguild competition for H. halys eggs by releasing a single species (one female T. japonicus or five female A. japonicus per cage) or both parasitoid species (one female T. japonicus and five female A. japonicus per cage) simultaneously in exclusion cages stocked with three host egg masses per cage in a kiwifruit orchard. Our results showed that the developmental time from eggs to adults of both parasitoids decreased with increased temperatures, between 15 °C and 30 °C, and T. japonicus developed much faster than A. japonicus during the immature stages in host eggs. Both T. japonicus and A. japonicus were able to parasitize a host already parasitized by the other parasitoid, and sex ratios of their offspring from multi-parasitized hosts were male-biased for both parasitoids. Inside host eggs, T. japonicus outcompeted A. japonicus when the time lags between the first and second attacks were less than or equal to 1 day, regardless of the order of attack by the two parasitoids, whereas A. japonicus began to dominate when the time lag was 2 to 5 d. The host location, exploitation and impact indexes of the two parasitoids were influenced by their exploitation modes and/or releases in the exclusion cage tests in the field. However, regardless of single or simultaneous release, the parasitism rates of the two parasitoids were not so much affected. We concluded that the combined release of T. japonicus and A. japonicus at the given parasitoid densities did not show any advantage compared to the single release of either species. The two parasitoids employed different reproductive strategies contributing to the outcome of their interspecific competition, which should be considered in any future biological control program for the sustainable management of H. halys.

Biological control of Halymorpha halys (Stål) (Hemiptera: Pentatomidae) in apple orchards versus corn fields and their adjacent woody habitats: High versus low pesticide-input agroecosystems

Halymorpha halys is an invasive pest in the USA that inflicts damage to specialty crops, and conventional growers have increased use of broad-spectrum insecticides to manage this pest. The impacts of pest management programs on natural enemies of H. halys were examined in high vs. low intensity insecticide input agroecosystems in western North Carolina (USA). Apple orchards and corn fields, with their adjacent wooded habitats, served as the high and low-input environments, respectively. Sentinel egg masses and yellow sticky cards were deployed in these agroecosystems to compare predation and parasitism on H. halys eggs, and presence, abundance, and richness of natural enemies. A total of approximately 85% of all sentinel eggs deployed in apple orchards in both 2018 and 2019 produced a healthy stink bug nymph, higher than all other habitats. A total of 26.6% and 32.9% of eggs deployed in wooded habitats bordering corn exhibited mortality due to natural enemy attack in 2018 and 2019, respectively. Comparatively, eggs deployed in apple borders had 10.0% and 17.8% of total eggs killed by natural enemies, in 2018 and 2019, respectively. Corn agroecosystems generally had greater predation and parasitism of sentinel eggs, and greater richness and abundance of predators detected on yellow sticky cards compared to apple agroecosystems. Wooded habitats bordering crops serve as population reservoirs for H. halys, allowing for egg laying and dispersal into crops. If these areas are protected as refuge areas free from insecticide drift, such as from apple orchards, they can also harbor thriving natural enemy populations that could reduce populations of H. halys. Wooded areas free from harsh broad-spectrum insecticides are an important component for successful conservation and augmentative biological control in neighboring crops.

Field collection of egg parasitoids of Pentatomidae and Scutelleridae in Northwest Italy and their efficacy in parasitizing Halyomorpha halys under laboratory conditions

AbstractThe invasion of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) has caused severe economic damage in crops in North America and Europe, motivating research to identify its natural enemies, both in native and invaded areas. In its Asian native range, the main natural enemies are egg parasitoids, among which the most effective are Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in China and Japan, respectively. In Europe, biology, host range, and impact of most native scelionid species are not well‐known. The present study aimed to investigate (1) presence and abundance of scelionid species that parasitize native Pentatomidae and Scutelleridae eggs in Northwest Italy, and (2) their ability to develop on H. halys eggs. During 4‐year field surveys, egg masses were collected and reared until bug nymph or adult parasitoid emergence. Then, the obtained scelionid females were tested for their ability to parasitize H. halys eggs in laboratory no‐choice experiments. Egg masses of all collected bug species were parasitized, and Telenomus spp. (Hymenoptera: Scelionidae), Trissolcus belenus (Walker), and Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) were the most common parasitoids. In the laboratory, Trissolcus kozlovi Rjachovskij was the only species to significantly produce offspring from fresh H. halys eggs, whereas all tested Trissolcus species significantly induced host egg abortion (non‐reproductive effects). This study provides knowledge of the parasitoid species associated with native bugs, and represents a starting point to investigate the intricate interactions between native and exotic parasitoids recently found in northern Italy. These egg parasitoids could potentially be effective biocontrol agents of H. halys.

Surveys in northern Utah for egg parasitoids of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) detect Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae).

The highly polyphagous and invasive brown marmorated stink bug, Halyomorphahalys (Stål) (Hemiptera: Pentatomidae), has become a significant insect pest in North America since its detection in 1996. It was first documented in northern Utah in 2012 and reports of urban nuisance problems and plant damage have since increased. Biological control is the preferred solution to managing H.halys in North America and other invaded regions due to its alignment with integrated pest management and sustainable practices. Native and non-native biological control agents, namely parasitoid wasps, have been assessed for efficacy. Trissolcusjaponicus (Ashmead) (Hymenoptera: Scelionidae) is an effective egg parasitoid of H.halys in its native range of southeast Asia and has recently been documented parasitising H.halys eggs in North America and Europe. Field surveys for native and exotic egg parasitoids using wild (in situ) and lab-reared H.halys egg masses were conducted in suburban and agricultural sites in northern Utah from June to September 2017–2019. Seven native wasp species in the families Eupelmidae and Scelionidae were discovered guarding H.halys eggs and adult wasps from five of these species completed emergence. Native species had low mean rates of adult emergence from wild (0.5–3.7%) and lab-reared (0–0.4%) egg masses. In 2019, an adventive population of T.japonicus was discovered for the first time in Utah, emerging from 21 of the 106 wild H.halys egg masses found that year, and none from lab-reared eggs. All T.japonicus emerged from egg masses collected on Catalpaspeciosa (Warder). Our results support other studies that have observed biological control of H.halys from T.japonicus and improved parasitoid wasp detection with wild as compared to lab-reared H.halys egg masses.

Variation in levels of acceptance, developmental success, and abortion of Halyomorpha halys eggs by native North American parasitoids

Using native North American parasitoid species (Hymenoptera: Scelionidae) that often unsuccessfully attack the eggs of the invasive brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), we assessed variation in traits that may determine the parasitoids’ ability to adapt to the invasive host by either exploiting or avoiding H. halys eggs (acceptance, developmental success). We also assessed variation in the parasitoids’ ability to induce H. halys host egg abortion, which may contribute to biological control of H. halys in invaded areas. The first set of experiments evaluated intra- and interspecific variation using standardized laboratory tests with iso-female lines of Telenomus podisi and Trissolcus euschisti that included matching of detailed behavioural observations of acceptance with developmental outcomes. In a second set of experiments, we assessed how variation in developmental ability and abortion induction may affect levels of biological control by indigenous parasitoid species. We examined a broader sample of parasitoids that emerged from field collections of egg masses of an indigenous north American stink bug Podisus maculiventris in a region newly invaded by H. halys. Results from the first set of experiments showed high levels of acceptance of H. halys eggs among iso-female lines of parasitoids, but offspring development success was almost zero. H. halys egg abortion due to unsuccessful parasitism was often very low and varied among iso-female lines only for T. podisi. In the second set of experiments we never observed increases in abortion levels of Halyomorpha halys eggs above natural levels, even for the two species (T. euschisti and T. podisi) that were observed to oviposit in and abort H. halys eggs in the first set of experiments. We conclude that while there may be some variation in behavioural and physiological parameters mediating acceptance and abortion of H. halys eggs by native North American egg parasitoids, there does not appear to be significant variation in developmental success. Moreover, current biological control impact of H. halys eggs via host egg abortion is likely very low.

Intrinsic competition between two European egg parasitoids of the brown marmorated stink bug

AbstractFollowing the accidental introduction and spread of the invasive polyphagous agricultural pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), the two European egg parasitoids Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae) have been investigated for inundative biological control. Since the competititve outcome between the two generalist parasitoids is difficult to predict, intrinsic competition was investigated with a time‐course development study. Both species readily oviposited in H. halys eggs containing eggs and early instar larvae of the competitor, but oviposition decreased when eggs contained late instar larvae and pupae. Ooencyrtus telenomicida offspring emergence from multiparasitized eggs was significantly lower than that from rearing controls, independent of the order of parasitization. Anastatus bifasciatus offspring emergence was not influenced by the presence of O. telenomicida when it parasitized as the first species, but emergence was decreased after oviposition in eggs containing O. telenomicida larvae and pupae. There was no indication that O. telenomicida can act as a facultative hyperparasitoid of A. bifasciatus. These results suggest that A. bifasciatus is the superior intrinsic competitor and no or minor negative implications for A. bifasciatus are expected if released in combination with O. telenomicida.

An Insight into the Role of Trissolcus mitsukurii as Biological Control Agent of Halyomorpha halys in Northeastern Italy

Sustainable strategies such as classical or augmentative biological control are currently being evaluated for the long-term management of the alien invasive pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). A three-year study carried out in northeastern Italy was performed to investigate the distribution and field performance of the H. halys egg parasitoid Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae), in comparison with other parasitoid species. In the study area, adventive populations of T. mitsukurii were present since 2016, representing the earliest detection of this species in Europe. Trissolcus mitsukurii was the most abundant parasitoid and showed a higher “parasitoid impact” (i.e., number of parasitized eggs over the total number of field-collected eggs) compared to the other species, i.e., Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae), Trissolcus basalis (Wollaston) and Trissolcus kozlovi Rjachovskij (Hymenoptera: Scelionidae). The hyperparasitoid Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) was also recorded. Phylogenetic analysis of T. mitsukurii population distinguished two clades, one covering samples from Italy, Japan and China, the other from South Korea. The present study provides promising results for the biological control of a pest that is having a dramatic impact on a wide range of crops worldwide.

Parasitism and predation of sentinel eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the southeastern US

The invasive brown marmorated stink bug, Halyomorpha halys, is present in the Piedmont and expanding into the Coastal Plains Regions of the southeastern US. Consequently, this study was conducted to evaluate parasitism and predation of H. halys sentinel egg masses by native parasitoids and predators in woodland habitats and orchard, vineyard, row, and vegetable crops alongside these habitats in Alabama and Georgia in 2017 and 2018. Ten primary parasitoid species, including two new records, and one hyperparasitoid emerged from eggs. Trissolcus japonicus was not detected. Ooencyrtus sp. was the prevalent parasitoid species in vegetables while Telenomus podisi was the predominant species in row crops. Anastatus reduvii, An. mirabilis, Tr. brochymenae, and Tr. euschisti were the prevalent species in woodland and orchard habitats. Trissolcus edessae Fouts occurred primarily in orchards. Trissolcus basalis and Gyron obesum were observed in vegetable habitats. Percentage successful development to adults, sex ratio, and percentage of parasitism per egg mass was highest for Tr. edessae. Predation damage included complete and incomplete chewing, stylet sucking, puncture sucking, and removal of whole eggs from egg masses. Hole and non-stylet sucking damage were discovered. Chewing and piercing-sucking predation constituted the majority of predation in woodlands, plum, blueberry, tomato, pecan, peach, and okra. Mainly chewing predation and egg removal occurred in soybean, cotton, and strawberry. Piercing-sucking predation was common in wine grape and apple. There was no difference between fresh and frozen eggs in the proportion of parasitism and predation both years. In 2017, overall percent parasitism was higher for blueberry compared to other crops except peach and apple. No differences were detected in 2018. Peak parasitism (72.3%) in apple at a site in 2017 represented the highest parasitism rate. Predation was highest in soybean and cotton. Indeed, predation in soybean reached very high levels in 2017 (96.3%) and 2018 (90.3%). In conclusion, native natural enemies parasitize and prey on H. halys egg masses in the southeastern US.