A modified DNA barcode approach to define trophic interactions between native and exotic pentatomids and their parasitoids

The establishment of invasive Halyomorpha halys (Stål) outside of its native range may impact native species assemblages, including other pentatomids and their scelionid parasitoids. This has generated interest in defining species diversity and host‐parasitoid associations in this system to better understand the impact of invasive alien species on trophic interactions in invaded regions. Information on scelionid–pentatomid associations in natural habitats is lacking, and species‐level identification of these associations can be tenuous using rearing and dissection techniques. Naturally occurring pentatomid eggs were collected in areas where H. halys has established in Canada and were analysed using a modified DNA barcoding approach to define species‐level trophic interactions. Identification was possible for >90% of egg masses. Eleven pentatomid and five scelionid species were identified, and trophic links were established. Approximately 70% of egg masses were parasitized; parasitism and parasitoid species composition were described for each species. Telenomus podisi Ashmead was the dominant parasitoid and was detected in all host species. Trissolcus euschisti Ashmead was detected in several host species, but was significantly more prevalent in Chinavia hilaris (Say) and Brochymena quadripustulata (Fabricius). Trissolcus brochymenae Ashmead and Tr. thyantae Ashmead were recorded sporadically. Parasitism of H. halys was 55%, and this species was significantly less likely to be parasitized than native pentatomids. The scelionid species composition of H. halys consisted of Te. podisi, Tr. euschisti and Tr. thyantae. Although these species cannot develop in fresh H. halys eggs, we demonstrate that parasitoids attempt to exploit this host under field conditions.     

Host discrimination and interspecific competition of Trissolcus nigripedius and Telenomus gifuensis (Hymenoptera: Scelionidae), sympatric parasitoids of Dolycoris baccarum (Heteroptera: Pentatomidae)

Trissolcus nigripedius Nakagawa and Telenomus gifuensis Ashmead (Hymenoptera: Scelionidae) are solitary egg parasitoids of Dolycoris baccarum L. (Heteroptera: Pentatomidae), a polyphagous seed-sucking bug of agricultural crops. Field examinations revealed that the two parasitoids are the most common species, but only a single species emerge from a host egg mass. To explain this observation we tested two hypotheses of interspecific host discrimination and asymmetry in competitive interaction between Tr. nigripedius and Te. gifuensis. Trissolcus nigripedius and Te. gifuensis could discriminate host egg pre-parasitized by either self or conspecific like other scelionid parasitoids that use external mark on host eggs. When provided with host eggs pre-parasitized by each other, both Tr. nigripedius and Te. gifuensis multiparasitized 94% and 100% of the host eggs without interspecific host discrimination, respectively. Interestingly, from the multiparasitized eggs irrespective of oviposition sequence, progeny of Te. gifuensis always survive better than Tr. nigripedius. Telenomus gifuensis is superior in immature competition probably due to shorter egg incubation period after oviposition, hence progeny of Te. gifuensis become first instar faster than that of Tr. nigripedius. However, adult Tr. nigripedius is always superior competitor in possessing and guarding the host eggs even after oviposition against Te. gifuensis. Therefore, the asymmetry in competitive interaction between Tr. nigripedius and Te. gifuensis may explain the emergence of a single species from a host egg mass in the field in spite of no interspecific host discrimination.     

Attack and Success of Native and Exotic Parasitoids on Eggs of Halyomorpha halys in Three Maryland Habitats

Egg parasitoids of the exotic invasive brown marmorated stink bug, Halyomorpha halys (Stål), were investigated using lab-reared fresh (live) and frozen (killed) lab-reared sentinel egg masses deployed for 72h on foliage in three habitats—woods, orchard, and soybean field—in Maryland, USA, in summer 2014. Four native hymenopteran species, Telenomus podisi Ashmead (Scelionidae), Trissolcus euschisti (Ashmead) and Tr. brochymenae Ashmead (Scelionidae), and Anastatus reduvii (Howard) (Eupelmidae), developed and emerged from H. halys eggs. One exotic parasitoid, Trissolcus japonicus (Ashmead), emerged, providing the first known occurrence of this species in North America. Native parasitoids emerged from frozen eggs significantly more often than from fresh eggs (89.3% of egg masses and 98.1% of individual eggs), whereas the exotic Tr. japonicus did not show a similar difference, strongly suggesting adaptation to H. halys as a host by Tr. japonicus but not by the native species. Parasitoids were habitat-specific: all three Trissolcus species were significantly more likely to occur in the woods habitat, whereas Te. podisi was found exclusively in the soybean field. Further investigations are required to elucidate evolving host-parasitoid relationships, habitat specificity, and non-target effects of Tr. japonicus over the expanded range of H. halys in North America.     

A temporal trophic shift from primary parasitism to facultative hyperparasitism during interspecific competition between two coevolved scelionid egg parasitoids

Understanding competition between scelionid parasitoids that exploit the same host may provide insight into strategies that allow coexistence on a shared resource. Competition studies typically focus on interactions between native and exotic parasitoids that do not share an evolutionary history; however, coevolved parasitoids may be more likely to demonstrate strategies to avoid or exploit a shared resource. We examined intrinsic and extrinsic competition between Asian Trissolcus japonicus (Ashmead) and T. cultratus (Mayr) (Hymenoptera: Scelionidae) associated with Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) that share an evolutionary history. Interspecific interactions were assessed by providing parasitized egg masses to each species at various intervals post‐parasitism, and measuring host acceptance, developmental suitability, and guarding behaviour. Trissolcus japonicus showed high acceptance of parasitized hosts up to 72 h following oviposition by T. cultratus, despite a very poor developmental outcome. In contrast, T. cultratus generally avoided ovipositing in H. halys eggs containing T. japonicus early‐instar larvae but did not avoid parasitizing H. halys that contained eggs and third instar larvae. The adaptive value of this behaviour was supported by developmental outcome: T. cultratus outcompeted T. japonicus eggs but not early‐instar larvae, and a trophic shift occurred wherein T. cultratus developed as a facultative hyperparasitoid on third instar T. japonicus larvae. Trissolcus japonicus guarded egg masses 8–12× longer and displayed more aggressive interactions than T. cultratus, suggesting T. japonicus is the superior extrinsic competitor. Development as a facultative hyperparasitoid provided a competitive niche for Asian T. cultratus and confirms its instrinsic competitive superiority. This also occurs in a biologically distinct European population of T. cultratus, suggesting that facultative hyperparasitism as a competitive strategy is retained in geographically separated populations that have not coevolved with H. halys or T. japonicus.     

Natural egg parasitism of Tibraca limbativentris Stal (Hemiptera: Pentatomidae) in rice crop in the State of Maranhão, Brazil

The rice stem bug, Tibraca limbativentris Stal, is an important pest of rice in Brazil. This work evaluated the occurrence of parasitoids in eggs of T.limbativentris egg parasitism in rice crops in the Maranh?o State. The eggs collected exhibited an average parasitism of 32%. The parasitoids collected were Telenomus podisi (Ashmead), Trissolcus urichi (Crawford) (Hymenoptera: Scelionidae) and Oencyrtus submetallicus (Howard) (Hymenoptera: Encyrtidae).     

A molecular tool to identify Anastatus parasitoids of the brown marmorated stink bug

Globally, Anastatus species (Hymenoptera: Eupelmidae) are associated with the invasive agricultural pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). In Europe, the polyphagous Anastatus bifasciatus (Geoffroy) is the most prevalent native egg parasitoid on H. halys eggs and is currently being tested as a candidate for augmentative biological control. Anastatus bifasciatus frequently displays behavior without oviposition, and induces additional host mortality through oviposition damage and host feeding that is not measured with offspring emergence. This exacerbates accurate assessment of parasitism and host impact, which is crucial for efficacy evaluation as well as for pre‐ and post‐release risk assessment. To address this, a general Anastatus primer set amplifying a 318‐bp fragment within the barcoding region of the cytochrome oxidase I (COI) gene was developed. When challenged with DNA of three Anastatus species —A. bifasciatus, Anastatus japonicus Ashmead, and Anastatus sp.—, five scelionid parasitoid species that might be encountered in the same host environments and 11 pentatomid host species, only Anastatus DNA was successfully amplified. When applied to eggs of the target host, H. halys, and an exemplary non‐target host, Dendrolimus pini L. (Lepidoptera: Lasiocampidae), subjected to host feeding, no Anastatus amplicons were produced. Eggs of the two host species containing A. bifasciatus parasitoid stages, from 1‐h‐old eggs to pupae, and emerged eggs yielded Anastatus fragments. Confirmation of parasitoid presence with dissections and subsequent PCRs with the developed primer pair resulted in 95% success for 1‐h‐old parasitoid eggs. For both host species, field‐exposed sentinel emerged eggs stored dry for 6 months, 100% of the specimens produced Anastatus amplicons. This DNA‐based screening method can be used in combination with conventional methods to better interpret host‐parasitoid and parasitoid‐parasitoid interactions. It will help address ecological questions related to an environmentally friendly approach for the control of H. halys in invaded areas.     

Multiple host use by the egg parasitoid Trissolcus basalis (Wollaston) in a soybean agricultural system: biological control and environmental implications

1 Species of bugs (Hemiptera: Pentatomidae and other families) that are parasitized by the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in the soybean agricultural system on the Darling Downs in south-eastern Queensland, Australia, are reported. The degree to which eggs of each bug species are used by T. basalis is quantified, which allows assessment of the role of these alternative host species in the biological control of the green vegetable bug Nezara viridula (L.). 2 Egg masses of nine species of pentatomid bugs and one unidentified bug species were collected. Parasitism rates of egg masses of all species averaged 50–70% but were significantly lower for the more important pest species, including the green vegetable bug, than for some of the agriculturally less important species. 3 Trissolcus basalis emerged from nearly all species collected and was the major parasitoid to emerge from most species. A number of native species were parasitized heavily by T. basalis and parasitism of such species may enhance biological control of the green vegetable bug, but may also pose environmental concerns. Parasitism of predatory bugs by T. basalis may have a negative impact on the biological control of other pests, especially lepidopterous pests. 4 Although the impact of T. basalis on native and predatory host species was not directly quantified, these host species remain abundant and therefore do not appear to be affected adversely by such high rates of parasitism.     

Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid

Host age is an important determinant of host acceptance and suitability for egg parasitoids. As host embryonic development advances, the quality of resources available to the parasitoid offspring typically declines, usually resulting in reduced acceptance levels by foraging females and lower offspring fitness. We examined the ability of the parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) to parasitize and develop in Podisus maculiventris (Say) (Hemiptera: Pentatomidae) eggs of different ages. In laboratory experiments, we measured the effect of host age (6, 24, 48, 72, 96, or 120 h old) on parasitism rate and offspring fitness parameters such as survival, development time, sex ratio, and size. Contrary to our expectations, parasitism rate did not differ between host age treatments, nor did sex ratio allocation, offspring size, or the fecundity of newly emerged female offspring. However, parasitoid offspring had a longer development time with increasing host age. This trend was stronger for males than for females, which we suggest could reduce the degree of protandry among offspring emerging from older host eggs, thus increasing the rate of virginity upon leaving the emergence patch and resulting in more frequent off‐patch mating by female offspring in nature. Overall, our results suggest that all stages of P. maculiventris embryonic development are suitable for acceptance and development of T. podisi. Unlike most species of egg parasitoids, T. podisi has evolved mechanisms to utilize host resources, regardless of host developmental stage, with relatively minor fitness consequences.     

Impacts of biological control and invasive species on a non-target native Hawaiian insect

The potential for classical biological control to cause unintended harm to native species was evaluated in the case of the endemic Hawaiian koa bug, Coleotichus blackburniae White (Hemiptera: Scutelleridae), and parasitoids introduced to Hawaii for control of an agricultural pest, the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae). Parasitism of C. blackburniae eggs, nymphs and adults by biocontrol agents was quantified across a wide range of habitats and compared to other sources of mortality. Egg mortality due to the biocontrol agent Trissolcus basalis Wollaston (Hymenoptera: Scelionidae) was low (maximum 26%) and confined to elevations below 500 m on a single host plant. Predation, mainly by alien spiders and ants, was the greatest source of egg mortality (maximum 87%). Parasitism of adult C. blackburniae by the biocontrol agent Trichopoda pilipes (F.) (Diptera: Tachinidae) was near zero at 21 of 24 sites surveyed. Three sites with high bug density had higher levels of T. pilipes parasitism, reaching maxima of 70% among adult female bugs, 100% among males and 50% among fifth instars. Male-biased parasitism indicated that T. pilipes is adapted to using male aggregation pheromone for finding C. blackburniae hosts. The relative impacts of biocontrol agents and other sources of mortality were compared using life tables. Invasive species, particularly generalist egg predators, had the greatest impacts on C. blackburniae populations. Effects of intentionally introduced parasitoids were relatively minor, although the tachinid T. pilipes showed potential for large impacts at individual sites. In retrospect, non-target attacks by biological control agents on C. blackburniae were predictable, but the environmental range and magnitude of impacts would have been difficult to foresee.     

Influence of visual cues on host‐searching and learning behaviour of the egg parasitoids Telenomus podisi and Trissolcus basalis

Insect parasitoids use a variety of chemical and physical cues when foraging for hosts and food. Parasitoids can learn cues that lead them to the hosts, thus contributing to better foraging. One of the cues that influence host‐searching behaviour could be colour. In this study, we investigated the ability of females of the parasitoid wasps Telenomus podisi Ashmead and Trissolcus basalis Wollaston (both Hymenoptera: Scelionidae) to respond to colours and to associate the presence of hosts – eggs of Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) – with coloured substrates after training (associative learning). Two sets of experiments were conducted: in one the innate preference for substrate colours was examined, in the other associative learning of substrate colour and host presence was tested in multiple‐choice and dual‐choice experiments. In the associative learning experiments, Te. podisi and Tr. basalis were trained to respond to differently coloured substrates containing hosts in two sessions of 2 h each, with 1‐h intervals. In multiple‐choice experiments, the wasps displayed innate preference for yellow substrates over green, brown, black, or white ones. Even after being trained on substrates of different colours, both parasitoids continued to show preference for yellow substrates. The response to the colours of substrates of both parasitoids was related with the orientation to the plant foliage during the search for hosts.     

An exotic parasitoid provides an invasional lifeline for native parasitoids

The introduction of an exotic species may alter food webs within the ecosystem and significantly affect the biodiversity of indigenous species at different trophic levels. It has been postulated that recent introduction of the brown marmorated stinkbug (Halyomorpha halys (Stål)) represents an evolutionary trap for native parasitoids, as they accept H. halys egg masses as a host but produce no viable progeny. Interspecific interactions between European egg parasitoid, Trissolcus cultratus (Mayr), and an Asian parasitoid, Trissolcus japonicus (Ashmead), were assessed by providing egg masses to T. cultratus at various time intervals following the initial parasitization by T. japonicus. The suitability of the host for the parasitoid development was re‐assessed by providing T. cultratus with fresh and frozen egg masses of various ages. The likelihood of T. cultratus being able to attack previously parasitized egg masses was determined by assessing the duration of egg mass guarding behavior by T. japonicus following parasitization. The results of experiments examining the interspecific interactions between a native European egg parasitoid, T. cultratus, and an Asian parasitoid, T. japonicus (a candidate for the biological control of H. halys), showed that the native species can act as facultative hyperparasitoid of the exotic one. Although this is only possible during certain stages of T. japonicus development, the presence of the introduced parasitoid may reduce the impact of the evolutionary trap for indigenous parasitoid species. There is a possibility that the occurrence of facultative hyperparasitism between scelionid parasitoids associated with stinkbugs is common. This resulting intraguild predation could promote conservation and stabilization of natural communities by impacting the diversity and population dynamics of native stinkbugs and their parasitoids (e.g., by allowing native parasitoids to avoid wasting reproductive effort on unsuitable hosts), or reduce success of biological control programs (e.g., by reducing the population size of the exotic parasitoids).     

The ovipositing female of Ooencyrtus telenomicida relies on physiological mechanisms to mediate intrinsic competition with Trissolcus basalis

Ongoing studies by our group showed that the outcome of the intrinsic competition between two solitary egg parasitoids, Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), is dominated by O. telenomicida. In this article we investigated the role played by the ovipositing O. telenomicida female in the suppression of a T. basalis competitor. Laboratory experiments were conducted by allowing an O. telenomicida female to puncture the eggs of Nezara viridula (L.) (Heteroptera: Pentatomidae) with her ovipositor (= no oviposition) or to parasitize them. The results show that O. telenomicida relies on some physiological mechanisms to mediate its interspecific intrinsic competition with T. basalis. In fact, the emergence of T. basalis was strongly reduced in host eggs that were parasitized either before or after being punctured by O. telenomicida at fixed time intervals (5, 15, 30, or 45 h). The low percentage of emergence of T. basalis (ranging from approximately 4–20%) was a consequence of the delay and growth rate reduction of larval development. Furthermore, the percentage of eclosion of N. viridula nymphs was negatively affected by the O. telenomicida female’s punctures (96% from healthy host eggs, 4% from punctured host eggs). Host eggs punctured or oviposited in by O. telenomicida showed alterations in the ooplasm including some melanized‐like areas near the hole made with the ovipositor; such alterations indicate that the adult parasitoid releases substances that affect the host eggs survival. These results suggest that the O. telenomicida female influences both the physiological interspecific parasitoid‐parasitoid interaction, as well as the host‐parasitoid interaction, providing, for the first time in egg parasitoids, evidence that physiological suppression of some competitive egg parasitoids is mediated by the ovipositing female.     

An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid

Invasive alien species can act as ‘evolutionary traps’ for indigenous parasites and predators when the alien species is accepted as prey or a host but is unsuitable for consumption or development. We tested the relationship between acceptance and suitability of eggs of the invasive alien Halyomorpha halys (Hemiptera: Pentatomidae) in North America relative to eggs of the indigenous Podisus maculiventris (Pentatomidae) for the indigenous generalist egg parasitoid Telenomus podisi (Hymenoptera: Scelionidae). T. podisi accepted 0–24 h old H. halys eggs at a rate similar to P. maculiventris eggs (87.5 ± 6.0 and 70.2 ± 9.1 %, respectively). Successful development of T. podisi occurred in 98.3 % of attacked P. maculiventris eggs, but was not observed in H. halys eggs. Oviposition by T. podisi did, however, reduce the developmental success of H. halys embryos relative to unattacked controls by 24.1 % in 0–24 h old eggs and 29.6 % in 24–48 h old eggs. We suggest that as H. halys spreads and increases in abundance in North America, it could operate as an evolutionary trap for indigenous egg parasitoids, thereby indirectly causing an increase in population levels of indigenous pentatomids. This predicted indirect effect would be a result of H. halys eggs acting as an egg sink for T. podisi. We also introduce the concept of a ‘time sink’, which may be particularly relevant for parasitoids such as T. podisi that spend considerable time protecting their reproductive investments.     

Surveying native egg parasitoids and predators of the invasive Halyomorpha halys in Northern Italy

The invasive Halyomorpha halys (Heteroptera: Pentatomidae) is a key pest of fruits in the Emilia‐Romagna region of Italy. For the development of a sustainable management programme, knowledge of its native natural enemy community and its efficacy is essential. A three‐year field survey was conducted exposing H. halys egg masses in different types of habitats to investigate the efficacy of native natural enemies in reducing the H. halys populations in the Emilia‐Romagna region, where the stinkbug was first detected in 2012. Over the first year of the study, sentinel eggs from laboratory cultures were stapled to the underside of leaves in various host trees, whereas in following years H. halys adults were directly caged on branches in sleeve cages to allow natural oviposition. Over the examined years, low rates of parasitism (1%–3%) and predation (2%–5%) were observed. Parasitism was caused exclusively by the generalist parasitoid Anastatus bifasciatus.     

茶翅蝽沟卵蜂和黄足沟卵蜂对茶翅蝽的寄生潜能研究

茶翅蝽Halyomorpha halys(Stl)是水果和蔬菜生产中的重要害虫。为了寻找优势卵寄生蜂用于其生物防治,本文进行了相关的野外调查和室内试验。通过定期野外采集茶翅蝽卵块,培育、收集和鉴定寄生蜂,发现在自然环境中茶翅蝽卵粒的寄生率为56.29%,其中茶翅蝽沟卵蜂比例最高,占77.66%;其次是黄足沟卵蜂占20.44%。Y型嗅觉仪测定结果显示,茶翅蝽沟卵蜂和黄足沟卵蜂对茶翅蝽卵均具有明显的选择趋性。室内寄生能力试验结果表明,茶翅蝽沟卵蜂与黄足沟卵蜂单独作用的寄生率分别为94.06%和84.21%,与两种寄生蜂混合寄生茶翅蝽卵的寄生率91.65%均无显著性差异。两种寄生蜂混合寄生时,茶翅蝽沟卵蜂与黄足沟卵蜂的寄生比例分别为58.95%和41.05%,二者之间无显著差异。     

Modelling the potential geographic distribution of <Emphasis Type="Italic">Trissolcus japonicus</Emphasis>: a biological control agent of the brown marmorated stink bug, <Emphasis Type="Italic">Halyomorpha halys</Emphasis>

Trissolcus japonicus Ashmead (Hymenoptera: Scelionidae) is an endoparasitoid of the eggs of the brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), a major agricultural pest native to China, Japan, South Korea and Taiwan. We used CLIMEX to estimate the potential global distribution of T. japonicus with particular reference to New Zealand. In its native range the model predicts the presence, or a potential expansion, of T. japonicus into most of humid-subtropical and humid-continental areas. Globally, the model projects that many temperate, Mediterranean and subtropical areas could suit the establishment of T. japonicus. In New Zealand, the north appears moderately to highly suitable for T. japonicus, while southern regions are mostly marginal. The risk posed by T. japonicus to non-target species in New Zealand is predicted to vary between different non-targets. CLIMEX projections of the potential distribution of T. japonicus provide guidance for release sites of this parasitoid if approved for importation and release in New Zealand.     

An evaluation of some natural enemies of >Nezara viridula in northern California

Natural enemies associated with eggs of >Nezara viridula (L.) (Heteroptera: Pentatomidae) wereevaluated by placing sentinel egg masses inweeds and cultivated tomato and bean crops innorthern California. Egg predation wasgenerally less than 10% and normally involvedpredators with chewing mouth parts. Predatorsseldom destroyed an entire egg mass, typicallyeating <40 eggs per exploited mass.Laboratory evaluation of >25 species ofpotential arthropod predators revealed that fewfed on >N. viridula eggs to any extent;however, numerous species fed on >N.viridula nymphs. Five species of eggparasites were recovered from sentinel eggmasses: >Trissolcus basalis (Wollaston),>Gryon obesum Masner and >Telenomuspodisi Ashmead (Scelionidae); and>Ooencyrtus californicus Girault and >O.johnsoni (Howard) (Encyrtidae). The major eggparasite was >T. basalis, the only exoticmember of the parasite guild; it typicallyparasitized 100% of the eggs in an exploitedegg mass. The results indicate thatparasitization of eggs and predation of smallnymphs can be important biotic mortalityfactors for >N. viridula populations innorthern California. It is suggested that acombination of factors – viz., eggparasitization, nymphal predation, regionalshortage of overwintering sites, and localshortages of suitable hosts – maintains thisexotic pest at relatively low levels in theregion.     

Parasitism and predation of stink bug (Heteroptera: Pentatomidae) eggs in Georgia corn fields

Nezara viridula L. and Euschistus servus (Say) are the predominant species of phytophagous stink bugs on corn, Zea mays L., in Georgia. Oebalus pugnax pugnax (F.) occurs in relatively low numbers, and the predatory stink bug Podisus maculiventris (Say) is commonly found. Limited information is available on natural biological control of these four stink bug species in Georgia corn fields; therefore, a 6-yr study of parasitism and predation of their eggs was initiated in 2003. Naturally occurring stink bug eggs were parasitized by six scelionid species, Trissolcus basalis (Wollaston), T. thyantae Ashmead, T. brochymenae (Ashmead), T. euschisti (Ashmead), Telenomus podisi Ashmead, Telenomus calvus Johnson, and one encyrtid species, Ooencyrtus sp. T. basalis was the most prevalent parasitoid of N. viridula, parasitizing E. servus and P. maculiventris eggs at low levels. T. podisi, the predominant parasitoid species emerging from eggs of E. servus and P. maculiventris, also parasitized O. p. pugnax eggs exclusively and parasitized N. viridula eggs at low levels. T. euschisti and T. thyantae parasitized E. servus egg masses. T. brochymenae parasitized eggs of both E. servus and P. maculiventris. T. calvus parasitized only P. maculiventris eggs. The same species of egg parasitoids that parasitized naturally occurring eggs of N. viridula and E. servus parasitized sentinel eggs of these bugs, except that no T. calvus and Ooencyrtus sp. were obtained from sentinel eggs, and T. thyantae and T. brochymenae emerged from sentinel eggs of N. viridula. Generally, parasitization of an egg mass was either greater than or equal to predation of sentinel eggs of N. viridula and E. servus. However, on some dates in late June and July, predation of sentinel egg masses was numerically approximately twice as high as parasitism. Results indicate stink bug egg parasitoids and predators are significant factors in the natural biological control of stink bugs in corn fields.     

Interspecific larval competition between two egg parasitoids in refrigerated host eggs of Riptortus pedestris (Hemiptera: Alydidae)

In a previous study, we found that soybean fields could be supplemented with refrigerated eggs of Riptortus pedestris (Fabricius) (Hemiptera: Alydidae) to enhance parasitism. As a part of a study to evaluate the effect of host egg refrigeration on parasitism, host acceptance behavior and interspecific larval competition between Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae) and Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) were studied in multiparasitized unrefrigerated and refrigerated eggs. O. nezarae showed complete host acceptance behavior when offered refrigerated host eggs that were preparasitized by G. japonicum. Adult emergence rate of O. nezarae was 43 and 74% when the interval between the first and second oviposition was 0 and 4 days, respectively, and was not different between refrigerated and unrefrigerated eggs. Refrigeration did not change host acceptance behavior of G. japonicum, but adult emergence declined from 80% in unrefrigerated eggs to 37% in refrigerated eggs that were pre-parasitized by O. nezarae on the same day. No negative effects of refrigeration on sex ratio, adult longevity, and adult size of the both parasitoids were found. Generally host egg refrigeration did not negatively affect host acceptance behavior of the both parasitoids on preparasitized eggs or larval competition between the two parasitoids in multiparasitized host eggs with exceptions in the development time and emergence rate of G. japonicum. Therefore, host egg refrigeration may not interrupt interactions between the parasitoid populations in the field.     

Influence of Host Pheromone on Egg Parasitism by Scelionid Wasps: Comparison of Phoretic and Nonphoretic Parasitoids

The kairomonal activity of the attractant pheromone for the spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae), was investigated by exposing fresh pentatomid egg masses in field traps with or without synthetic pheromone. Predominantly two parasitoids were recovered from exposed eggs of P. maculiventris and Euschistus obscurus: Telenomus podisi Ashmead (a generalist pentatomid egg parasitoid) and Telenomus calvus Johnson (a phoretic specialist on Podisus eggs) (Hymenoptera: Scelionidae). The incidences of T. podisi from P. maculiventris and E. obscurus eggs placed in pheromone-baited and nonbaited traps were not significantly different, suggesting that this oophagous wasp does not use the spined soldier bug attractant pheromone as a kairomone. However, T. calvus was reared almost exclusively from egg masses of P. maculiventris placed inside pheromone-baited traps. These results suggest that T. calvus females orient to volatile chemicals emitted by spined soldier bug males as a searching strategy to find areas likely to contain host eggs, in addition to the previously discovered strategy of using the pheromone to guide their phoretic behavior. The data also indicate that T. calvus can distinguish between the egg masses of these pentatomid hosts at close range.