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

The 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.     

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).     

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 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.     

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.     

Effect of resistant and susceptible soybean cultivars on the attraction of egg parasitoids under field conditions

The association of resistant crop varieties and biological pest control has great potential for pest management, as resistant cultivars may affect herbivore population dynamics by interfering with their biology and search behaviour for host plants. In addition, resistant varieties can also affect the efficiency of natural enemies. The aims of this work were to evaluate the influence of the soybean cultivars Dowling (resistant), IAC 100 (resistant) and Silvânia (susceptible) under field conditions on: (i) the abundance of parasitoids in the Platygastridae family and the stink bug Euschistus heros and (ii) the parasitism of stink bug eggs by these natural enemies. There was no difference between cultivars in stink bug distribution in the field. The parasitoids Telenomus podisi, Trissolcus teretis, Tr. urichi and Tr. brochymenae emerged from the sentinel eggs of E. heros, and T. podisi was the most abundant species observed during the reproductive stage R6. The cultivars Dowling and IAC 100 attracted a higher number of Platygastridae parasitoids, T. podisi and Tr. teretis, and the abundance of these parasitoids during the period from R1 to R7 might have being sufficient to control the stink bug population. These results suggest that the cultivars Dowling and IAC 100 have important attributes that should be taken into account in the implementation and development of new cultivars in breeding programmes that aim to obtain plants more resistant to stink bugs and more attractive to natural enemies.     

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.     

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 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.     

Multiparasitism of Piezodorus guildinii eggs by Telenomus podisi and Trissolcus urichi

Multiparasitism involves competition between larvae inside the host. Telenomus podisi (Ashmead) and Trissolcus urichi (Crawford) (Hymenoptera: Platygastridae) are solitary egg parasitoids of Piezodorus guildinii Westwood (Hemiptera: Pentatomidae), an important soybean pest. Egg masses partially parasitized by one species were offered to females of the other species. Both species attacked randomly unparasitized and parasitized hosts. Emergence from multiparasitized eggs was greater for T. urichi than for T. podisi, although it was lower than emergence from eggs parasitized by T. urichi alone. Emergence of each species was independent of the order in which they parasitized and of time elapsed between ovipositions. Progeny sex ratio obtained from multiparasitized and from parasitized eggs were similar for both parasitoids. Our results suggest that T. urichi is a better intrinsic competitor than T. podisi for P. guildinii eggs. In the field, however, T. podisi was the dominant species, and T. urichi could be using other pentatomid eggs as resource.     

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.     

Performance of Ooencyrtus kuvanae (Hymenoptera: Encyrtidae) on two host species,Halyomorpha halys and Philosamia ricini

The brown marmorated stink bug, Halyomorpha halys, is an invasive agricultural pest of fruit trees and vegetables. Egg parasitoids play a key role in the reducing of H. halys populations. Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) can parasitize H. halys and complete its life cycle in this host species. Many factors can influence this parasitoid–host relationship. Of these factors, we evaluated the effect of female age, exposure time, and host species on the biological characteristics and fecundity of O. kuvanae reared on eggs of H. halys as well as another previously known host Philosamia ricini (Lepidoptera: Saturniidae). In this study, we used a 3-year-old laboratory colony of O. kuvanae. Parasitism rates positively affected by exposure time in P. ricini. The highest parasitism rates were obtained in 5- and 7-day-old females of both hosts. The highest emergence rates were recorded on P. ricini for 5- and 7-day-old female P. ricini (81.8% and 84.8%, respectively). The development time of O. kuvanae ranged from 18.4 to 19.1 days on H. halys and 17.7 to 18.3 days on P. ricini. The longevity of O. kuvanae that were provided honey was 38.5 and 47.8 days on H. halys and P. ricini, respectively. The longevity of O. kuvanae that were not provided honey was 2.3 and 2.8 days on H. halys and P. ricini, respectively. The sex ratio was male-biased (36.5% female) on H. halys and female-biased (55.2% female) on P. ricini. Fecundity of O. kuvanae was 37.7 and 59.6 progeny per female for H. halys and P. ricini, respectively. The performance of O. kuvanae was lower when compared with its performance on the host P. ricini. Our results suggest that O. kuvanae has potential as new biological control agent for H. halys.     

Selective responses of Trissolcus basalis and Telenomus podisi to chemical footprints of preferred hosts

Chemical trails of the hosts (footprints) are important cues for the host searching behaviour of egg parasitoids of the family Scelionidae. The present study aims to determine the influence of the footprints of three neotropical stink bugs (Euchistus heros, Dichelops melacanthus and Nezara viridula) on the foraging behaviour of two parasitoids, Trissolcus basalis and Telenomus podisi, as well as a possible selective response to fooprints of their preferred hosts. Accordingly, Tr. basalis and Te. podisi females are allowed to forage on open arenas where E. heros, D. melacanthus or N. viridula had walked or on open arenas that had been treated with samples of an extract from each stink bug's footprints. Hexane extracts of stink bug footprints are obtained from solvent-washed Petri dishes where insects were allowed to walk for 24 h, and these extracts were analyzed by gas chromatography-flame ionization detection and gas chromatography-mass spectrometry. Each parasitoid responds selectively to the footprints of their preferred host (Tr. basalis to footprints of N. viridula and Te. podisi to footprints of E. heros). Twenty-six compounds comprising of C18 to C35 (saturated and unsaturated) and methyl branched hydrocarbons were identified in extracts of E. heros, D. melacanthus and N. viridula, respectively. There are significant differences in the total amount of the compounds identified in the footprint stink bug's extracts and also a difference in the amounts of individual compounds. In addition, the behavioural assays showed that footprints of stink bugs are stimuli that are used by egg parasitoids to search, discriminate and selectively locate their preferred host.     

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.     

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.     

The invasive stink bug Halyomorpha halys affects the reproductive success and the experience-mediated behavioural responses of the egg parasitoid Trissolcus basalis

Invasive species, because of their lack of co-evolutionary history with recipient communities, can act as “evolutionary traps” causing disconnects between natural enemy behavioural responses and the suitability of the invasive species as a prey/host resource. Invasion of exotic species in non-native environments may have several ecological effects, including consequences for the experience-mediated behavioural responses of indigenous foragers. Experience is usually thought to help resident species to buffer against negative impacts of new invasive species, including escaping from evolutionary traps. Here we hypothesized that the impact of foraging experience depends on whether an indigenous egg parasitoid can correctly assess the resource suitability of a new invasive species for offspring development. We showed that the invasive stink bug Halyomorpha halys acts as an evolutionary trap for the indigenous egg parasitoid Trissolcus basalis leading to unsuccessful development of?~?95% of the eggs laid in this host species. In a mixed scenario in which the associated resident stink bug Nezara viridula co-occurs with the invasive H. halys, we showed that oviposition experience in the low quality invasive host induces in T. basalis similar responses to those of the associated host. These results suggest that foraging experience does not lead to avoidance of an evolutionary trap. We discuss parasitoid foraging experience and reproductive success in the light of the evolutionary trap framework with implication for biological control.

     

Food web associations and effect of trophic resources and environmental factors on parasitoids expanding their host range into non‐native hosts

Trophic interactions and environmental conditions determine the structure of food webs and the host expansion of parasitoids into novel insect hosts. In this study, we investigate plant–insect–parasitoid food web interactions, specifically the effect of trophic resources and environmental factors on the presence of the parasitoids expanding their host range after the invasion of Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae). We also consider potential candidates for biological control of this non‐native pest. A survey of larval stages of Plusiinae (Lepidoptera: Noctuidae) and their larval parasitoids was conducted in field and vegetable greenhouse crops in 2009 and 2010 in various locations of Essex and Chatham‐Kent counties in Ontario, Canada. Twenty‐one plant–host insect–host parasitoid associations were observed among Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), C. chalcites, and larval parasitoids in three trophic levels of interaction. Chrysodeixis chalcites, an old‐world species that had just arrived in the region, was the most common in our samples. The larval parasitoids Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae), Cotesia vanessae (Reinhard), Cotesia sp., Microplitis alaskensis (Ashmead), and Meteorus rubens (Nees) (all Hymenoptera: Braconidae) expanded their host range into C. chalcites changing the structure of the food web. Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae) was the most common parasitoid of T. ni that was not found in the invasive species. Plant species, host abundance, and agro‐ecosystem were the most common predictors for the presence of the parasitoids expanding their host range into C. chalcites. Our results indicate that C. sonorensis, C. vanessae, and C. floridanum should be evaluated for their potential use in biological control of C. chalcites and T. ni.     

Differential induction of volatiles in rice plants by two stink bug species influence behaviour of conspecifics and their natural enemy Telenomus podisi

Tritrophic interactions mediated by semiochemicals have been intensively studied from the viewpoint of ecological relationships with Nearctic tritrophic organisms. However, there are few studies involving interactions with different herbivores on the same host plant in Neotropical systems. The objective of the current study was to investigate the effects of herbivory by two species of stink bugs (Heteroptera: Pentatomidae) with the same feeding habit – Tibraca limbativentris Stål and Glyphepomis spinosa Campos & Grazia – on indirect and direct defence strategies of rice plants. The responses of each stink bug species (virgin and mated females) and of their main natural enemy, the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Platygastridae; mated females), to volatiles from undamaged and herbivore-damaged rice plants were evaluated using a Y-tube olfactometer. The results showed that rice plants responded differently to T. limbativentris or G. spinosa herbivory, enhancing the production of a different blend of volatile compounds, which reduced the attraction for conspecific stink bugs and elicited the foraging behaviour of T. podisi.     

Species richness and parasitism in an assemblage of parasitoids attacking maize stem borers in coastal Kenya

Abstract. 1. Parasitoids were reared from four species of lepidopteran stem borer collected in maize in southern coastal Kenya from 1992 to 1999. The stem borers included three native species, Sesamia calamistis Hampson, Busseola fusca Fuller, and Chilo orichalcociliellus (Strand), and one exotic borer, Chilo partellus (Swinhoe). A total of 174 663 caterpillars was collected, of which 12 645 were parasitised.
2. Twenty-six primary parasitoid species were reared from the exotic borer, C. partellus , indicating a rapid accumulation of native parasitoids on the alien borer.
3. The three most abundant parasitoids were the larval parasitoids Cotesia sesamiae Cameron, Cotesia flavipes (Cameron), and the pupal parasitoid Pediobius furvus Gahan. The pupal parasitoid Dentichasmias busseolae Heinrich and the larval parasitoid Goniozus indicus Ashmead were also common. All used an ingress-and-sting method of attack.
4. Cotesia flavipes , introduced into Kenya in 1993, was found in all seasons from 1997 onwards, and has become the most abundant stem borer larval parasitoid in the area. A native congener, Cotesia sesamiae , appeared in all seasons from 1992 to 1999. Together, these two parasitoids accounted for 83.3% of the parasitised borers.
5. Thirty parasitoid species were recovered in Kilifi district, 27 in Kwale, and 15 in Taita Taveta. Parasitism was much greater in Taita Taveta district than in Kilifi or Kwale districts.     

Storage of Pentatomid Eggs in Liquid Nitrogen and Dormancy of Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Platygastridae) Adults as a Method of Mass Production

The eggs of pentatomid species were evaluated to parasitism by Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead after storage in liquid nitrogen. Adults which emerged from stored eggs were kept at 18°C for 120 and 180 days to investigate whether adult dormancy could be associated with host egg storage in liquid nitrogen as a method of mass production of these egg parasitoids. Eggs of Nezara viridula (L.) and Acrosternum pengue (Rolston) were successfully parasitized by T. basalis, as well as Piezodorus guildinii (Westwood) and Dichelops furcatus (F.) by T. podisi. The eggs of Edessa meditabunda (F.) were not parasitized by T. basalis. The emergence of T. podisi from eggs of Euschistus heros (F.) and Podisus nigrispinus (Dallas) stored for 6 months was lower than the control. Females of T. basalis and T. podisi that emerged from stored eggs were kept in dormancy at 18°C. Longevity of T. basalis was influenced by the storage time and sex, but not by the interaction of sex and storage time. For T. podisi, longevity was influenced by the storage time, sex, and by the interaction of sex and storage time. For T. basalis, storage in liquid nitrogen did not affect the fecundity of quiescent females, while the number of parasitized eggs by T. podisi decreased after storage. By the joint use of these techniques, it is possible to optimize mass production of T. basalis so that its life cycle can be monitored and synchronized with the life cycle and availability of hosts.