Diversity and Low Parasitism of Egg Parasitoids Associated with Maize (Zea mays) in Madura, Indonesia

The cotton leafhopper, Amrasca biguttula Ishida (Hemiptera: Cicadellidae), is a significant pest that feeds on various host plants, particularly cotton, resulting in substantial annual economic losses. Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) is an effective parasitoid that targets the eggs of various pests preventing them from hatching into harmful larvae. Its ability to be mass-reared makes it a popular choice as biological control agent in integrated pest management programs worldwide. The presence of the bacterium Wolbachia, an intracellular symbiont found in arthropods, has a profound impact on the biology of their hosts. This research examined Wolbachia strain diversity in both species using seven genes: wsp, 16S rRNA, and five housekeeping MLST genes. Additionally, the molecular identification of A. biguttula and its egg parasitoid, T. chilonis was also accomplished through the use of the cytochrome c oxidase subunit I (COI) gene. Phylogenetic exploration based on 16S rRNA, wsp, and multilocus sequence typing (MLST) revealed that A. biguttula anchorages two new Wolbachia strains along with another Wolbachia strain in its egg parasitoid, T. chilonis from supergroup (B) We enumerated Wolbachia strains in A. biguttula from both study locations in Pakistan, identifying distinct strains wAbig1 and wAbig2 for A. biguttula and wTchiB for T. chilonis. Wolbachia amplification in A. biguttula showed infection rates of 29% to 66% across seven genes, with the highest rates in Bahawalpur, followed by Faisalabad. Ten adult samples of the egg parasitoid T. chilonis from each locality were also tested, revealing infection rates of 50% to 90%, again highest in Bahawalpur. This is the first report of Wolbachia in A. biguttula populations, detecting high Wolbachia prevalence and suggesting vertical transmission. Although no additional strains were identified beyond those mentioned in the present research, further research should investigate the potential for additional strains within these populations. Wolbachia bacteria are important for pest management as they suppress pest populations, reduce disease transmission in vectors and provide pathogen resistance to hosts, while potentially increasing pest susceptibility to insecticides. As a sustainable and species-specific alternative to chemical pesticides, Wolbachia offers environmentally friendly control strategies for pests like planthoppers.

The generalist entomopathogenic fungus, Metarhizium brunneum, has proved to have great potential as a versatile biological pest control agent. The gall midge Aphidoletes aphidimyza is a specialist predator that occurs naturally in Europe and has been successfully used for aphid suppression. However, the interaction between these two biological control organisms and how it may affect the biological control of aphids awaits further investigation. As part of the EU-supported project INBIOSOIL, this study was conducted in greenhouse conditions to assess the possible effects of combining both biological control agents. In a randomized complete block design, sweet corn (Zea mays var. saccharata) plants were grown in large pots filled with natural soil or natural soil inoculated with M. brunneum. At the third leaf stage, before being individually caged, plants were infested with Rhopalosiphum padi and A. aphidimyza pupae were introduced in the soil. Aphidoletes aphidimyza midge emergence, number of living midges and number of aphids were recorded daily. The presence of conidia in the soil and on leaves was assessed during the experiment. At the conclusion of the experiment, the number of live aphids and their developmental stage, consumed aphids, and A. aphidimyza eggs was assessed under stereomicroscope. This study’s findings showed that the presence of M. brunneum did not affect A. aphidimyza midge emergence. However, longevity was significantly affected. As the study progressed, significantly fewer predatory midges were found in cages treated with M. brunneum compared to untreated cages. Furthermore, by the end of the study, the number of predatory midges found in the Metarhizium-treated cages was four times lower than in the untreated cages. Both daily and final count of aphids were significantly affected by treatment. Aphidoletes aphidimyza applied alone suppressed the aphid population more effectively than M. brunneum applied alone. Additionally, the aphid population was most suppressed when both agents were combined, though the suppression was less than additive.

Abstract. Herlinda S, Suwandi S, Irsan C, Adrian R, Fawwazi F, Akbar F. 2023. Species diversity and abundance of parasitoids of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) from South Sumatra, Indonesia. Biodiversitas 24: 6184-6190. The parasitoid species attacking Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) have never been reported from South Sumatra. The objectives of this research were to identify and analyze the species diversity of egg and larval parasitoids of S. frugiperda and to determine their abundance in corn fields from South Sumatra. Surveys were carried out in Ogan Komering Ilir District, Ogan Ilir District, Muara Enim District, and Palembang City. The results showed that fourteen species of parasitoids were found attacking eggs and larvae of S. frugiperda in South Sumatra. Two species were egg parasitoids (Telenomus remus (Nixon) and Trichogramma sp.), and 12 species of larval parasitoids (Chelonus formosanus Sonan, Chelonus oculator F., Chelonus annulipes Wesm., Chelonus cautus (Cresson), Microplitis manilae Ashmead, Microplitis marshallii Kokujev, Euplectrus corriemoreauae Hansson, Compsilura concinnata (Meigen), Sarcophaga sp., Macrocentrus sp., Exorista sp., and Megaselia sp.). The most abundant species of the parasitoids found was T. remus. The highest species diversity was found in Muara Enim District. The number of parasitoid species was greater in the dry season compared to the rainy season. Egg parasitism rates were significantly higher at the corn vegetative stage (59.03%) compared to the generative stage (53.56%).

Fungal entomopathogens are widespread in nature and contribute to the natural regulation of insects. They can be exploited for pest management as biological control agents of pests in attempts to improve the sustainability of crop protection. Four types of biological control are recognized: classical, inoculation, inundation, and conservation biological control. Classical biological control is the intentional introduction and permanent establishment of an exotic biological agent for long-term pest management. Inoculation biological control is the intentional release of a living organism as a biological control agent with the expectation that it will multiply and control the pest for an extended period, but not permanently. Inundation biological control is the release of large numbers of mass-produced biological control agents to reduce a pest population without necessarily achieving continuing impact or establishment. Conservation biological control is a modification of the environment or existing practices to protect and enhance specific natural enemies or other organisms to reduce the effect of pests. The traditional and the most popular approach in biological control with entomopathogenic fungi has been to apply the fungal material to the cropping system (as biopesticide), using an inundation biological control strategy. The term biopesticide is used for microbial biological pest control agents that are applied in a similar manner to chemical pesticides. The use of biopesticides can substitute for some (but not all) chemicals and provide environmentally safe and sustainable control of pests but EU legislation and prohibitive registration costs are discouraging the development and commercialization of many promising new products.

Biological control of exotic invasive plants using exotic insects is practiced under the assumption that biological control agents are safe if they do not directly attack non-target species. We tested this assumption by evaluating the potential for two host-specific biological control agents (Urophora spp.), widely established in North America for spotted knapweed (Centaurea maculosa) control, to indirectly elevate Sin Nombre hantavirus by providing food subsidies to populations of deer mice (Peromyscus maniculatus), the primary reservoir for the virus. We show that seropositive deer mice (mice testing positive for hantavirus) were over three times more abundant in the presence of the biocontrol food subsidy. Elevating densities of seropositive mice may increase risk of hantavirus infection in humans and significantly alter hantavirus ecology. Host specificity alone does not ensure safe biological control. To minimize indirect risks to non-target species, biological control agents must suppress pest populations enough to reduce their own numbers.

The greenhouse cucumber pests, Bemisia tabaci (Hemiptera: Aleyrodidae), Frankliniella occidentalis (Thysanoptera: Thripidae), and Tetranychus urticae (Acari: Tetranychidae), are major threats to the production of greenhouse cucumbers (Cucurbitaceae) in Lebanon. The development of insecticide resistance by these pests has prompted the use of alternative and sustainable pest management strategies. In this study, we used integrated pest management strategies, including the release of the biological control agents, Amblyseius swirskii Athias-Henriot (Mesostigmata: Phytoseiidae) and Phytoseiulus persimilis Athias-Henriot (Mesostigmata: Phytoseiidae), to control whitefly, thrips, and two-spotted spider mite populations on greenhouse cucumber plants in two commercial production sites (sites A and B). We also compared the efficacy of pest population suppression using the integrated pest management strategy with that of chemical pest control. Our results show that biological control effectively maintains the cucumber pest populations below the economic threshold when coupled with additional integrated pest management measures. In addition, we show that biological control agents were equally or more effective in pest population suppression compared to eight and 12 insecticidal and acaricidal sprays performed in the control greenhouses at sites A and B, respectively. Altogether, our results show the efficacy of adopting integrated pest management and biological control for pest population suppression in greenhouse cucumber production under Mediterranean environmental conditions.

Plants under herbivore attack synthetize defensive organic compounds that directly or indirectly affect herbivore performance and mediate other interactions with the community. The so-called herbivore-induced plant volatiles (HIPVs) consist of odors released by attacked plants that serve as important cues for parasitoids and predators to locate their host/prey. The understanding that has been gained on the ecological role and mechanisms of HIPV emission opens up paths for developing novel strategies integrated with biological control programs with the aim of enhancing the efficacy of natural enemies in suppressing pest populations in crops. Tactics using synthetic HIPVs or chemically/genetically manipulating plant defenses have been suggested in order to recruit natural enemies to plantations or help guiding them to their host more quickly, working as a "synergistic" agent of biological control. This review discusses strategies using HIPVs to enhance biological control that have been proposed in the literature and were categorized here as: (a) exogenous application of elicitors on plants, (b) use of plant varieties that emit attractive HIPVs to natural enemies, (c) release of synthetic HIPVs, and (d) genetic manipulation targeting genes that optimize HIPV emission. We discuss the feasibility, benefits, and downsides of each strategy by considering not only field studies but also comprehensive laboratory assays that present an applied approach for HIPVs or show the potential of employing them in the field.

Simple SummaryThe golden twin-spot moth, Chrysodeixis chalcites, is a pest whose larvae cause serious skin injuries to banana fruits in the Canary Islands, reducing their commercial value. The use of Integrated Pest Management (IPM) strategies (cultural, biological, and chemical control) is recommended for the effective and sustainable management of this pest. The identification of its parasitoids and the quantification of their effects on pest populations are essential for the development of biological controls. In this study, we conducted an extensive survey to identify the most important parasitoid species of Ch. chalcites and evaluated the efficacy of the egg parasitoid Trichogramma achaeae as a biological control agent in banana plantations in the Canary Islands. Our findings indicate that populations of native parasitoids can exert a certain degree of natural control over Ch. chalcites. However, their naturally occurring populations are insufficient to minimize the damage caused by this pest. Thus, the development of IPM programs based on the use of selective insecticides, the conservation of natural enemies and inundative releases of mass-reared wasps is also necessary. The parasitoid T. achaeae has been identified as a promising biological control agent of Ch. chalcites in greenhouse banana crops, but it is necessary to carry out further studies to establish the most appropriate release strategies.Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae) is a significant pest in banana plantations in the Canary Islands. Field surveys were carried out to identify its naturally occurring parasitoids and estimate their parasitism rates between September 2007 and October 2010. Ch. chalcites was parasitized by six different larval/pupal parasitoid species: Cotesia sp., C. glomerata L. (Hym.: Braconidae), Aplomyia confinis Fallén (Dip.: Tachinidae), Hyposoter rufiventris Perez, Ctenochares bicolorus L. (Hym.: Ichneumonidae) and Aleiodes sp. (Hym.: Braconidae). Among them, Cotesia sp. was the most frequent species, accounting for 8.18% of parasitized larvae. High levels of egg parasitism were detected, with Trichogramma achaeae Nagaraja and Nagarkatti (Hym.: Trichogrammatidae) being the most widely distributed egg parasitoid. A greenhouse assay was also carried out on a commercial banana crop with the aim of evaluating the potential of T. achaeae as a biological control agent and compared with a chemical control. Five periodic inundative releases of 35 adults/m2 every 21 days were necessary to achieve an adequate parasitism level (56.25 ± 1.61%). Moreover, there was 15.75% less foliar damage in the biological control plot compared to the chemical control plot. These results indicate that T. achaeae could be a promising biocontrol agent of Ch. chalcites in greenhouse banana crops.

Opinions about the value of biological control are often extreme. Colloquially, biological control most often refers to classical biological control, in which one species is introduced from another region to control pests such as arthropod herbivores in agricultural systems, or weeds in managed and natural systems.1 As such, biological control has the potential to be a low-cost, chemical free, means to control pests. Numerous biological control programs have been unqualified successes (Bellows 2001), such as the control of cacti in Australia with the moth Cactoblastis cactorum (Raghu and Walton 2007), of cottony-cushion scale (Icerya purchasi) in California with the vedalia lady beetle, Rodolia cardinalis (Caltagirone and Doutt 1989), and of glassy-winged sharpshooters in French Polynesia with the egg parasitoid Gonatocerus ashmeadi (Grandgirard et al. 2009). Yet, classical biological control, as with any introduction of a species into a new area, necessarily involves the unknown and therefore carries some inherent risk (Simberloff and Stiling 1996) – what will these organisms actually do in a novel ecosystem? The most unpredictable element in biological control is the extent to which the realized niche is modified in the new environment. This effect has been responsible for some disastrous outcomes of classical biological control, many of which occurred during an era when vertebrates were being introduced around the world by Europeans for a variety of reasons (e.g., introducing the birds of Shakespeare to America, Mirsky 2008), including for biological control (Howarth 1991). The introductions as biological control agents of cane toad to Australia (Crossland et al. 2000) and mongoose to Hawaii (Hays and Conant 2007) are notorious. Introductions of generalist invertebrate agents also have had dire consequences, such as the introduction of predatory snails to French Polynesia (Murray et al. 1988; Coote 2007). In retrospect, some of the unintended consequences of biological control could have been avoided with more ecological knowledge (McEvoy and Coombs 2000) or more societal appreciation for native species (which has developed with time, Henneman and Memmott 2001), but with other introductions, it would have been impossible to know ahead of time what the risks would be (e.g., gall fly agents of knapweeds providing supplementary food to mice that harbor hantavirus, Pearson and Callaway 2006). Many of the unknown outcomes of biological control are purely ecological – what is the risk that a wasp, introduced to parasitize an agricultural pest, will also be able to feed on a native insect? Other unknowns involve evolution – will a herbivore adapt over time to be able to feed on a new nontarget host or hybridize with a closely related species? This volume explores the evolutionary aspects of biological control. Although often overlooked, evolutionary considerations are critical to all stages of classical biological control, from agent selection, to quarantine, release, establishment, and ultimately success in pest control (Ehler et al. 2004). Many questions are unresolved. For example, should agents be chosen that have a long history with the host or are ‘new associations’ more likely to succeed (Hokkanen and Pimentel 1989)? Can one improve effectiveness through artificial selection (Hopper et al. 1993)? Will postcolonization adaptation of the agent increase the likelihood of success, and/or are hosts equally likely to evolve resistance over time (Roderick 1992; Holt and Hochberg 1997; Hufbauer 2001)? Are generalist consumers more likely to survive in novel environments or are specialists more effective (Murdoch et al. 1985; Waage 1990; Brodeur 2012)? More recently, concern for the environment, as well as theory examining the reasons for success of generalist predators, prompted a shift to the release of specialized consumers typically preceded by extensive testing aimed at delimiting the host range of candidate biological control agents. While this approach has clearly made biological control more predictive ecologically, research focused on host range currently lacks measures of genetic variation in host use and responses of those hosts, and thus evolutionary uncertainties remain.

Intraguild predation and prey preferences influence biological control of Paropsis charybdis by the southern ladybird, Cleobora mellyi

Little is known about the biological control of insect pests that transmit plant pathogenic bacteria such as phytoplasmas. This chapter is a review of the status of the biological control of the corn leafhopper Dalbulus maidis DeLong (Hemiptera: Cicadellidae), an efficient vector of maize (Zea mays ssp. mays L., Poaceae) pathogens in the Neotropic region. The chapter reviews the biodiversity of parasitoids that attack the corn leafhopper in the Americas and relates the efforts conducted to understand the interactions among D. maidis- phytoplasmas-parasitoids-environment. Nymphs and adults of the corn leafhopper are parasitized by hymenopteran, dipteran, and strepsipteran species, with Gonatopus bartletti Olmi (Hymenoptera: Dryinidae) being the most common species, whereas eggs of the corn leafhopper are parasitized by hymenopterans, with Anagrus incarnatus Haliday (Hymenoptera: Mymaridae) and Paracentrobia sp. Howard (Hymenoptera: Trichogrammatidae) being the most common species. Knowledge of the transmission biology of phytoplasma is a key factor to identify parasitoid species that could be used as biological agents and to determine the best environmental conditions that will favor parasitoid population and their use as biological control. Maize bushy stunt phytoplasma (MBSP (Ca. Phytoplasma asteris)) has a long latent period in D. maidis, meaning that the most common parasitoids are able to complete their life cycle before the vector transmits the plant pathogen and can therefore be used as biological control. As well, maize edges growing during winter harbor a high diversity of leafhoppers and none of the leafhopper species sampled in those edges have been found to be positive for MBSP. These edges have a high diversity of nymph-adult parasitoids and egg parasitoids that attack the corn leafhopper, not only during winter but also during the maize growing season, meaning that habitat management such as field edges, is an important part of the biological control of corn leafhopper.

Biological control provides a sustainable and environmentally friendly alternative to chemical methods for managing agricultural pests. Wheat, as a major global crop, faces significant threats from pest infestations and requires effective management strategies. This study conducted a meta-analysis to evaluate the effectiveness, sustainability, and influencing factors of biological control strategies for wheat pests. The role of key control factors such as parasitic wasps, predatory insects, entomopathogenic fungi, and bacteria in suppressing pest populations was analyzed, emphasizing the advantages of biological control over chemical methods, especially in terms of long-term sustainability and ecological benefits. It was found that climate conditions, crop management practices, and interactions with local biodiversity have a significant impact on the success of biological control work. Case studies from specific wheat planting areas demonstrated the practical application and challenges of implementing biological strategies, introduced new biological control agents, integrated with precision agriculture, and the potential for policy interventions to improve the effectiveness of biological control in wheat pest management. The sentence is:. This study aims to emphasize the importance of promoting biological control as the cornerstone of sustainable agriculture.

Spodoptera frugiperda (fall armyworm, FAW) is a significant economic pest of maize in Uganda. Many Ugandan maize farmers employ synthetic insecticides as their main form of control despite the negative impacts of these chemicals. We tested the effectiveness of Beauveria bassiana; General Biopesticide Cocktail (mixture of B. bassiana, M. anisopliae, Isaria fumosoroseus, Lecanicillium lecani and Purporeocillium lilacanus three strains of Metarhizium anisopliae, Nimbecidine® (azadirachtin 0.03%EC), and Roket® (cypermethrin 4% and profenofos 40%); and Amdocs® (emamectin benzoate 2% and abamectin 1%) on fall armyworm and parasitoids, respectively, in 2020 and 2021. The treatments with the greatest decrease in leaf damage and infestation were Amdocs® and Roket®, followed by Nimbecidine®. The biopesticides were not always more effective than the untreated control, though; their efficacy was often lower than that of the synthetic and botanical pesticides. We recovered one egg parasitoid, Telenomus remus, and seven egg and egg-larval parasitoids (Coccygidium luteum, Coccygidium sp., Cotesia icipe, Chelonus sp., Micranisa sp., Charops cf. diversipes, and an unidentified Tachinidae). Among these, C. cf diversipes, Chelonus sp., C. luteum, C. icipe and the Tachinidae were the most abundant. Parasitism was low, averaging 10% for egg masses and 5.3% for larvae. Application of synthetic pesticides and Nimbecidine® often resulted in higher yield when compared with the untreated control. In general, a low population of parasitoids was observed. Although the parasitoid population reduced in plots treated with Amdocs® and Roket®, the percentage of parasitism of FAW was not affected. In some instances, higher yields were realized in untreated control when compared with the treated plots. Pest management practices more compatible with biological control need to be considered for the management of fall armyworm.

Laterally acquired chitinase genes in venom facilitate parasitism in egg parasitoid wasps.

Simple SummaryRearing of many hymenopteran egg parasitoids requires a reliable supply of host eggs. The parasitoid Paratelenomus saccharalis can be reared on eggs produced from field collected kudzu bug, Megacopta cribraria, however field-collected hosts obtained during reproductive diapause do not readily produce eggs and must be reared under a long day-length photoperiod to terminate diapause. In this study we found that an exogenous application of pyriproxyfen was able to terminate diapause, leading to a significant increase in egg production. The eggs produced by pyriproxyfen-treated M. cribraria were accepted by the egg parasitoid Paratelenomus saccharalis, however parasitoid emergence was reduced when compared to eggs from untreated hosts. When the effects of pyriproxyfen treatment on egg production and parasitoid emergence were evaluated together, the net increase in parasitoid yield due to pyriproxyfen treatment was approximately 87%. This method has the potential to increase parasitoid yield and reduce production costs in egg parasitoid rearing programs.The mass rearing of hymenopteran egg parasitoids requires an abundant supply of host eggs. The onset of reproductive diapause and subsequent decline in egg production poses a challenge for parasitoid rearing when using host colonies augmented by field-collected insects. We investigated the application of pyriproxyfen, a juvenile hormone analog, to induce oviposition in diapausing adult kudzu bugs, Megacopta cribraria (Fabricius) (Heteroptera: Plataspidae), and the use of eggs produced by pyriproxyfen-treated kudzu bugs to rear the egg parasitoid, Paratelenomus saccharalis (Dodd) (Hymenoptera: Scelionidae). The effects of pyriproxyfen and photoperiod treatments on host mortality, egg production, and rates of parasitoid eclosion from the eggs were used to calculate the parasitoid yield for the different treatment regimes. A combination of pyriproxyfen and a long-day photoperiod increased the parasitoid yield by 87% compared to acetone and a long-day photoperiod. The general applicability of JH-analog mediated egg production for parasitoid rearing is discussed.