Non-target effects of ten essential oils on the egg-parasitoid Trichogramma evanescens

Essential oils (EOs) are increasingly used as biopesticides due to their insecticidal potential. This study addresses their non-target effects on a biological control agent: the egg parasitoid Trichogramma evanescens. In particular, we tested whether EOs affected parasitoid fitness either directly, by decreasing pre-imaginal survival, or indirectly, by disrupting parasitoids' orientation abilities. The effect of Anise, Fennel, Sweet orange, Basil, Coriander, Oregano, Peppermint, Mugwort, Rosemary and Thyme EOs were studied on five strains of T. evanescens. Specific experimental setups were developed, and data obtained from image analysis were interpreted with phenomenological models fitted with Bayesian inference. Results highlight the fumigant toxicity of EOs on parasitoid development. Anise, Fennel, Basil, Coriander, Oregano, Peppermint and Thyme EOs are particularly toxic and drastically reduce the emergence rate of T. evanescens. Most EOs also affect parasitoid behavior: (i) Basil, Coriander, Oregano, Peppermint, Mugwort and Thyme EOs are highly repellent for naive female parasitoids; (ii) Anise and Fennel EOs can have repellent to attractive effects depending on strains; and (iii) Sweet orange, Oregano and Rosemary EOs have no detectable impact on orientation behavior. This study shows that EOs fumigation have non-target effects on egg parasitoids. This highlights the need to cautiously precise the deployment framework of biopesticides in an agroecological perspective.

Effects of Constant versus Fluctuating Temperatures on Fitness Indicators of the Aphid Dysaphis plantaginea and the Parasitoid Aphidius matricariae

Testing fluctuating rather than constant temperatures is likely to produce more realistic datasets, as they are ecologically more similar to what arthropods experience in nature. In this study, we evaluated the impact of three constant thermal regimes (7, 12, and 17 °C) and one fluctuating thermal regime (7–17 °C with a mean of 12 °C) on fitness indicators in the rosy apple aphid Dysaphis plantaginea, a major pest of apple orchards, and the parasitoid Aphidius matricariae, one of its natural enemies used in mass release biological control strategies. For some—but not all—traits, the fluctuating 7–17 °C regime was beneficial to insects compared to the constant 12 °C regime. Both aphid and parasitoid development times were shortened under the fluctuating regime, and there was a clear trend towards an increased longevity under the fluctuating regime. The fecundity, mass, and size were affected by the mean temperature, but only the mass of aphids was higher at 7–17 °C than at a constant 12 °C. Parasitism rates, but not emergence rates, were higher under the fluctuating regime than under the constant 12 °C regime. Results are discussed within the framework of insect thermal ecology and Jensen’s inequality. We conclude that incorporating thermal fluctuations in ecological studies could allow for the more accurate consideration of how temperature affects host–parasitoid interactions and insect responses to temperature change over time.

Limited host range in the idiobiont parasitoid Phymasticus coffea, a prospective biological control agent of the coffee pest Hypothenemus hampei in Hawaii

Phymastichus coffea LaSalle (Hymenoptera:Eulophidae) is an adult endoparasitoid of the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera:Curculionidae:Scolytinae), which has been introduced in many coffee producing countries as a biological control agent. To determine the effectiveness of P. coffea against H. hampei and environmental safety for release in Hawaii, we investigated the host selection and parasitism response of adult females to 43 different species of Coleoptera, including 23 Scolytinae (six Hypothenemus species and 17 others), and four additional Curculionidae. Non-target testing included Hawaiian endemic, exotic and beneficial coleopteran species. Using a no-choice laboratory bioassay, we demonstrated that P. coffea was only able to parasitize the target host H. hampei and four other adventive species of Hypothenemus: H. obscurus, H. seriatus, H. birmanus and H. crudiae. Hypothenemus hampei had the highest parasitism rate and shortest parasitoid development time of the five parasitized Hypothenemus spp. Parasitism and parasitoid emergence decreased with decreasing phylogenetic relatedness of the Hypothenemus spp. to H. hampei, and the most distantly related species, H. eruditus, was not parasitized. These results suggest that the risk of harmful non-target impacts is low because there are no native species of Hypothenemus in Hawaii, and P. coffea could be safely introduced for classical biological control of H. hampei in Hawaii.

The Effects of Temperature and Host Stage on Development Rate of Parasitoids of Giant Whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae)

The effects of rearing temperature and host stage parasitized on the development of three parasitoid species; Encarsia noyesi Hayat (Hymenoptera: Aphelinidae), Idioporus affinis LaSalle & Polaszek (Hymenoptera: Pteromalidae), and Entedononecremnus krauteri Zolnerowich & Rose (Hymenoptera: Eulophidae) were investigated. These parasitoids are part of the biological control program for the giant whitefly Aleurodicus dugesii Cockerell (Hemiptera: Aleyrodidae) in the United States. Temperature and host-dependent development was assessed for each species using the nonlinear Brière-1 model and simple linear regression to obtain critical thermal parameters. All three parasitoids successfully developed at constant temperatures ranging from 15°C to 30°C, which was narrower to their predicted thermal limits due to thermal constraints of A. dugesii. There were significant effects of both temperature and A. dugesii nymphal stage parasitized on immature parasitoid development times. All three parasitoid species’ development time decreased as nymphal stage age increased. Thermal tolerance limits and development times varied by parasitoid species. The results of these findings in the context of biological control potential are discussed.

Influence of “protective” symbionts throughout the different steps of an aphid–parasitoid interaction

Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e., from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum, and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid–symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola, two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid–symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host–parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect–symbiont associations.

Behavioral and Developmental Responses of Habrobracon hebetor (Hymenoptera: Braconidae) to Larvae of Helicoverpa armigera (Lepidoptera: Noctuidae) Inoculated With Various Concentrations of Bacillus thuringiensis var. kurstaki (Bacillales: Bacillacae)

Bacillus thuringiensis Berliner subsp. kurstaki (Btk) and Habrobracon hebetor Say are both biological control agents of Helicoverpa armigera Hubner. The present study evaluated their compatibility for combined application against this pest by examining the acceptability of Btk-inoculated hosts for H. hebetor females and testing for negative life-history impacts on developing progeny. Second-instar H. armigera larvae fed for 72 h on potted chickpea plants treated with three concentrations of Btk (LC15, LC35, and LC70) and were then used in bioassays of parasitoid development and parasitism behavior. Survival of parasitoids was significantly reduced, and immature development prolonged, on hosts fed chickpea plants treated with LC35 and LC70 Btk, but not on plants treated with LC15 Btk. Parasitoids failed to discriminate against hosts treated with LC15 or LC35 Btk in choice tests, but attacked fewer hosts treated with LC70 Btk, paralyzing and parasitizing more healthy hosts, and laying more eggs on them. In contrast, a no-choice test revealed that more hosts treated with LC35 and LC70 Btk were paralyzed compared with control or LC15-treated hosts, but the numbers of hosts parasitized and eggs laid did not vary among Btk treatments. Thus, females required an experience with healthy hosts, as they had in the choice test, to discriminate against diseased ones. We conclude that H. hebetor and Btk are compatible for joint application against H. armigera, which could potentially improve biological control of this pest.

Beyond host regulation: Changes in gut microbiome of permissive and non-permissive hosts following parasitization by the wasp Cotesia flavipes

ABSTRACT Koinobiont parasitoids regulate the physiology of their hosts, possibly interfering with the host gut microbiota and ultimately impacting parasitoid development. We used the parasitoid Cotesia flavipes to investigate if the regulation of the host would also affect the host gut microbiota. We also wondered if the effects of parasitization on the gut microbiota would depend on the host–parasitoid association by testing the permissive Diatraea saccharalis and the non-permissive Spodoptera frugiperda hosts. We determined the structure and potential functional contribution of the gut microbiota of the fore-midgut and hindgut of the hosts at different stages of development of the immature parasitoid. The abundance and diversity of operational taxonomic units of the anteromedial (fore-midgut) gut and posterior (hindgut) region from larvae of the analyzed hosts were affected by parasitization. Changes in the gut microbiota induced by parasitization altered the potential functional contribution of the gut microbiota associated with both hosts. Our data also indicated that the mechanism by which C. flavipes interferes with the gut microbiota of the host does not require a host-parasitoid coevolutionary history. Changes observed in the potential contribution of the gut microbiota of parasitized hosts impact the host's nutritional quality, and could favor host exploitation by C. flavipes.

Using Gamma Irradiated Galleria mellonella L. and Plodia interpunctella (Hübner) Larvae to Optimize Mass Rearing of Parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae)

We evaluated possible improvements to the mass rearing of the larval parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae) on irradiated host wax moth Galleria mellonella L. and Indian meal moth Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae) larvae. The use of irradiated G. mellonella and P. interpunctella larvae at the dose of 150 Gy proved useful for enhancing the parasitism and adult emergence of H. hebetor due to the absence of negative repercussions on parasitoid development. Overall, parasitism was increased as the host larvae was irradiated with higher doses, while significantly higher parasitism was recorded at 150 and 300 Gy compared to lower doses. The female parasitoids preferred the irradiated larvae and significantly higher numbers of larvae were parasitized compared with non-irradiated larvae. The results also showed that irradiated larvae of G. mellonella served better as hosts for H. hebetor as compared with irradiated larvae of P. interpunctella. The implementation of these findings would be helpful for improving the mass production of parasitoids and the effectiveness of releases of biocontrol agents for the control of stored product pests.