Telenomuscristatus Johnson (Hymenoptera, Scelionidae): new diagnostic data, distribution records and host associations.

Specimens of an egg parasitoid wasp, Telenomuscristatus Johnson (Platygastroidea, Scelionidae), were reared from stink bug egg masses collected in the wild, in Maryland, United States. The egg masses were identified morphologically as Halyomorphahalys (Stål), Banasa Stål and Euschistus Dallas (Hemiptera, Pentatomidae). Molecular tools were used to further identify the Euschistus egg masses as E.servus (Say) and E.tristigmus (Say). All of these are new host associations for Te.cristatus. We also provide data to contribute to future identification of Te.cristatus: images of the holotype specimen and COI sequences from two disparate localities.

A revised terminology for male genitalia in Hymenoptera (Insecta), with a special emphasis on Ichneumonoidea.

Applying consistent terminology for morphological traits across different taxa is a highly pertinent task in the study of morphology and evolution. Different terminologies for the same traits can generate bias in phylogeny and prevent correct homology assessments. This situation is exacerbated in the male genitalia of Hymenoptera, and specifically in Ichneumonoidea, in which the terminology is not standardized and has not been fully aligned with the rest of Hymenoptera. In the current contribution, we review the terms used to describe the skeletal features of the male genitalia in Hymenoptera, and provide a list of authors associated with previously used terminology. We propose a unified terminology for the male genitalia that can be utilized across the order and a list of recommended terms. Further, we review and discuss the genital musculature for the superfamily Ichneumonoidea based on previous literature and novel observations and align the terms used for muscles across the literature.

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.

Key innovations and the diversification of Hymenoptera.

The order Hymenoptera (wasps, ants, sawflies, and bees) represents one of the most diverse animal lineages, but whether specific key innovations have contributed to its diversification is still unknown. We assembled the largest time-calibrated phylogeny of Hymenoptera to date and investigated the origin and possible correlation of particular morphological and behavioral innovations with diversification in the order: the wasp waist of Apocrita; the stinger of Aculeata; parasitoidism, a specialized form of carnivory; and secondary phytophagy, a reversal to plant-feeding. Here, we show that parasitoidism has been the dominant strategy since the Late Triassic in Hymenoptera, but was not an immediate driver of diversification. Instead, transitions to secondary phytophagy (from parasitoidism) had a major influence on diversification rate in Hymenoptera. Support for the stinger and the wasp waist as key innovations remains equivocal, but these traits may have laid the anatomical and behavioral foundations for adaptations more directly associated with diversification.

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.

Preempting the Arrival of the Brown Marmorated Stink Bug, Halyomorpha halys: Biological Control Options for Australia.

The brown marmorated stink bug Halyomorphahalys (Stål) (Hemiptera: Pentatomidae) is native to Northeast Asia, but has become a serious invasive species in North America and Europe, causing major damage to crops. While it has not established itself in Australia, it has been intercepted at the border several times, indicating that future incursions and establishment are a case of when, not if. Biological control is one of the few control options for this species and will be important for managing H.halys should it become established in Australia. Prioritizing species that could be used as biological control agents would ensure Australia is prepared. This study summarizes the literature on natural enemies of H. halys in its native and invaded ranges and prioritizes potential biological control agents of H.halys that could be used in Australia. Two egg parasitoid species were identified: Trissolcusjaponicus (Ashmead) and Trissolcusmitsukurii (Ashmead) (Hymenoptera: Scelionidae). Future efforts to develop biological control should focus on T. mitsukurii, as it is already present in Australia. However, little is known about this species and further work is required to: (1) assess its potential effectiveness in parasitizing H. halys, (2) determine its current distribution and (3) host range in Australia.

Molecular Identification of Trissolcus japonicus, Parasitoid of the Brown Marmorated Stink Bug, by Species-Specific PCR.

The samurai wasp, Trissolcus japonicus (Ashmead), has been proposed as a biocontrol agent against brown marmorated stink bugs (BMSB), due to its ability to parasitize and kill BMSB eggs. However, the wasps' small size makes it challenging for those untrained in morphological identification to determine the wasps' species. To circumvent this problem, a molecular method was created to identify T. japonicus. The method uses species-specific primers, designed in this study, which target the variable region of the mitochondrial Cytochrome Oxidase 1 (CO1) locus. After confirming successful DNA extraction from samples, the PCR amplification using our primers produced 227-bp PCR products for all T. japonicus specimens and no amplification in other microhymenoptera candidates. Additionally, DNA from BMSB-parasitized eggs gave positive PCR amplification, while the control BMSB samples showed no amplification. This indicates that PCR with our primers specifically and sensitively differentiates T. japonicus specimens from other similar wasp species and discriminates between T. japonicus-parasitized and non-parasitized BMSB eggs. Finally, an in silico analysis of CO1 sequences demonstrated that our primers match the sequences of four different haplotypes of T. japonicus, indicating that our diagnostic method could potentially be applied to analyze T. japonicus populations throughout North America, Europe, and parts of Asia.

Seasonal Captures of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) and the Effects of Habitat Type and Tree Species on Detection Frequency.

Trissolcus japonicus, an important egg parasitoid of Halyomorpha halys in Asia, was first detected in the USA in 2014. To evaluate the effect of habitat and the seasonality of T. japonicus detections in the USA, yellow sticky traps were placed in the canopy of Ailanthus altissima growing at the edge of isolated patches of trees, windbreaks, and woodlots in northern Virginia in 2018 and 2019. In both years, captures occurred from May to September, and peaked in July and August. While T. japonicus was detected in all habitats, there was not a consistent effect of habitat type on capture frequency. To evaluate tree species effects on T. japonicus captures, in 2017 and 2018, yellow sticky traps deployed in the canopy of A. altissima bordering apple orchards were paired with a nearby trap in one of several wild tree species along a common woods edge. In 2019, these traps were deployed in A. altissima, black walnut, and black locust growing in the same windbreaks. No consistent association between captures of T. japonicus or native parasitoids of H. halys and the tree species sampled was observed among years. Results are discussed in relation to the ecology and sampling optimization of T. japonicus.

Influence of Holding Conditions and Storage Duration of Halyomorpha halys (Hemiptera: Pentatomidae) Eggs on Adventive and Quarantine Populations of Trissolcus 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.

Identification and expression of chemosensory receptor genes in the egg parasitoid Trissolcus basalis.

Parasitic wasps largely rely on chemosenses to locate resources. Understanding the evolution of their chemoreceptors can help elucidate the mechanisms underlying host adaptation and speciation. Trissolcus basalis is a biological control agent of the southern green stink bug, a pantropical pest, and is ideal for investigating the evolution of chemoreceptors. We identified 34 gustatory receptors, 170 odorant receptors, one odorant co-receptor, and 23 ionotropic receptors. Comparison with other Hymenoptera revealed species-specific expansions of 21 Grs and 53 Ors. Most of these Or expansions have 9 exons. Gender- and tissue-specific analyses showed that 5 Grs and 54 Ors are expressed only in antennae in both sexes, 66 Ors in female antennae only, and 4 Ors in male antennae alone. The identification and expression profile of chemosensory receptor genes in T. basalis helps in understanding the link between the evolution of chemoreceptors and speciation in parasitic wasps.

Phanuromyia ricaniae Nam, Lee Talamas sp. n. (Hymenoptera: Scelionidae) reared from the eggs of Ricania shantungensis Chou Lu (Hemiptera: Ricaniidae) in Asia.

The genus Phanuromyia in the subfamily Telenominae (Hymenoptera: Scelionidae) consists of 60 described species, for which host records indicate they are egg parasitoids of lanternflies and planthoppers (Hemiptera: Auchenorrhyncha). In this study, we describe a new species of the genus, P. ricaniae sp. n., reared from the eggs of a planthopper, Ricania shantungensis Chou Lu (Hemiptera: Ricaniidae). This planthopper has been considered as a serious invasive pest in South Korean agriculture. Ricania shantungensis has a wide host range, including economically important crops such as apple, peach, and pear. Phanuromyia ricaniae therefore has the potential to be a biological control agent against ricaniid planthoppers.

Parasitoids of Chrysopidae Eggs in Sinaloa Mexico.

The eggs parasitoids Myartsevaia chrysopae (Crawford) (Hymenoptera: Encyrtidae), Telenomus lobatus Johnson, Telenomus tridentatus Johnson (Hymenoptera: Scelionidae) and Trichogramma atopovirilia Oatman and Platner (Hymenoptera: Trichogrammatidae) are reported for the first time or in new localities in Mexico. Their occurrence was first discovered in 2018 during a survey of parasitism on chrysopid eggs, conducted on Sorghum bicolor L. Moench (Poales: Poaceae) and Zea mays L. (Poales: Poaceae) in different locations in Sinaloa, Mexico. The identity of the parasitoids was determined by morphology and for both species of Telenomus the barcode region of the cytochrome oxidase 1 gene (CO1) was generated to facilitate molecular diagnosis of these species in future studies.

Gryon ancinla Kozlov & Lê (Hymenoptera: Scelionidae): host association, expanded distribution, redescription and a new synonymy.

BACKGROUND: Gryon Haliday (Platygastroidea: Scelionidae) is a cosmopolitan genus of egg-parasitoid wasps primarily associated with Heteroptera. NEW INFORMATION: Gryon ancinla Kozlov & Lê is reported for the first time outside of Vietnam, in China and Cambodia, and as an egg parasitoid of the pestiferous leaf-footed bug, Acanthocoris scaber (L.). Gryon ancinla is redescribed based on recently collected specimens and compared to closely related species of Gryon in the region. Gryon clavaerus Kozlov & Lê is treated as a junior synonym and some characters found in the charon species group are discussed.

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.

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, Halyomorpha halys (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. Trissolcus japonicus (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 Catalpa speciosa (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.

Notes on the hosts of Trissolcus Ashmead (Hymenoptera: Scelionidae) from China.

BACKGROUND: Trissolcus Ashmead (Hymenoptera: Scelionidae) is a cosmopolitan genus of egg-parasitoid wasps associated with stink bugs (Pentatomidae, Scutelleridae, Urostylididae), many of which are important insect pests. Documentation of host associations for these wasps, which we here provide via museum specimens, can support their use as biological control agents of invasive stink bugs. NEW INFORMATION: The hosts of seven Trissolcus species are reported from China: Trissolcus cultratus (Mayr) (hosts: Hippotiscus dorsalis Stål, Pentatomidae; Urochela luteovaria Distant, Urostylididae), Trissolcus elasmuchae (Watanabe) (host: Niphe elongata (Dallas), Pentatomidae), Trissolcus japonicus (Ashmead) (hosts: Erthesina fullo (Thunberg), Pentatomidae; Rhaphigaster nebulosa (Poda), Pentatomidae), Trissolcus latisulcus (Crawford) (host: Poecilocoris latus Dallas, Scutelleridae), Trissolcus mitsukurii (Ashmead) (host: Pentatomidae), Trissolcus semistriatus (Nees von Esenbeck) (host: Eurydema sp., Scutelleridae), Trissolcus yamagishii Ryu (host: Niphe elongata (Dallas), Pentatomidae).

A fortuitous find: a unique haplotype of Ooencyrtus nezarae Ishii (Encyrtidae: Encyrtinae) discovered in Florida.

The adventive arrival of biological control agents circumvents the regulatory process by introducing exotic species to control invasive pests and is generally followed by post hoc risk evaluation. The bean plataspid, Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), is an invasive pest of leguminous crops in the south-eastern United States that was eventually followed by two parasitoid wasps from its range in the eastern hemisphere, Paratelenomus saccharalis (Dodd) (Scelionidae) and Ooencyrtus nezarae Ishii (Encyrtidae). In North Central Florida, sentinel egg masses, intended to capture Paratelenomus saccharalis, instead yielded Ooencyrtus nezarae, which was previously known only from Alabama (Ademokoya et al. 2018). Two generations of O. nezarae were subsequently reared in the laboratory. COI sequences from the Florida population of O. nezarae differed by 1.3% from the Alabama population and the presence of a different haplotype suggests the possibility of a separate introduction. Laboratory parasitism rates, sex ratios, morphology, molecular diagnosis and implications for agriculture are discussed.

First record of Trissolcus basalis (Hymenoptera: Scelionidae) parasitizing Halyomorpha halys (Hemiptera: Pentatomidae) in the United States.

BACKGROUND: A parasitoid wasp, Trissolcus basalis (Wollaston), was recorded parasitizing eggs of the invasive stink bug Halyomorpha halys (Stål) in the United States. This is the first record of this species parasitizing fresh and frozen eggs of H. halys in the United States. NEW INFORMATION: First record of Trissolcus basalis parasitizing Halyomorpha halys eggs in the United States.

New record of Trissolcus solocis (Hymenoptera: Scelionidae) parasitising Halyomorpha halys (Hemiptera: Pentatomidae) in the United States of America.

BACKGROUND: A parasitoid wasp, Trissolcus solocis Johnson, was recorded parasitising eggs of the invasive stink bug Halyomorpha halys (Stål), in the United States. This is the first record of this species parasitising eggs of H. halys. NEW INFORMATION: First record of Trissolcus solocis parasitising Halyomorpha halys eggs in the United States and first record of T. solocis in Alabama.

Vertical Sampling in Tree Canopies for Halyomorpha halys (Hemiptera: Pentatomidae) Life Stages and its Egg Parasitoid, Trissolcus japonicus (Hymenoptera: Scelionidae).

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is an invasive agricultural and nuisance pest that has established across much of the United States and caused significant crop losses in the Mid-Atlantic region. While it has been monitored extensively using ground-deployed pheromone traps, the vertical distribution of its life stages in the canopy of wild tree hosts has not been examined. In Virginia, small pyramid traps baited with 'low-dose' H. halys pheromone lures were deployed via a pulley system at the lower, mid-, and upper canopy of female tree of heaven (Ailanthus altissima (Mill.) Swingle) in 2016 and 2017 and male A. altissima and hackberry (Celtis occidentalis L.) in 2017. Weekly captures of adults and nymphs were recorded throughout each season. Each year, additional female A. altissima trees were felled during the two main periods of H. halys oviposition. The number and relative locations of all pentatomid egg masses found on foliage were recorded and any parasitoids that emerged from them were identified. Halyomorpha halys adults and nymphs were captured in greatest numbers in upper canopy traps and in lowest numbers in traps near the tree base. More H. halys egg masses were collected from mid-canopy than from the lower or upper canopy. The adventive egg parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), emerged most frequently from egg masses found at mid-canopy and was not recovered from those in the lower canopy. Results are discussed in relation to the foraging ecology of H. halys and its natural enemies, including TT. japonicus.