Earwig Releases Provide Accumulative Biological Control of the Woolly Apple Aphid over the Years.

Nature-based solutions, such as biological control, can strongly contribute to reducing the use of plant protection products. In our study, we assessed the effect of augmentative releases of the European earwig (Forficula auricularia) to control the woolly apple aphid (Eriosoma lanigerum), a worldwide pest that causes serious damage to apple trees. The trials were carried out in two organic apple orchards located in Catalonia (NE Spain) from 2017 to 2020. Two treatments were compared: with vs. without earwig release. For the treatment, 30 earwigs per tree were released by means of a corrugated cardboard shelter. These releases were performed once per season and were repeated every year. We periodically assessed the length of the woolly apple aphid colonies, the number of colonies per tree, the percentage of aphids parasitized by Aphelinus mali, and the number of earwigs per shelter. Our results showed that earwig releases reduced the length of the colonies, but this effect was noticeable only for the second year onwards. Moreover, we found that those releases were compatible with A. mali. Overall, we demonstrated the positive impact of earwig releases on the woolly apple aphid control and the importance of considering time on augmentative biological control strategies.

Honeydew Is a Food Source and a Contact Kairomone for Aphelinus mali.

Many parasitoids need to feed on sugar sources at the adult stage. Although nectar has been proven to be a source of higher nutritional quality compared to honeydew excreted by phloem feeders, the latter can provide the necessary carbohydrates for parasitoids and increase their longevity, fecundity and host searching time. Honeydew is not only a trophic resource for parasitoids, but it can also constitute an olfactory stimulus involved in host searching. In this study, we combined longevity measurements in the laboratory, olfactometry and feeding history inference of individuals caught in the field to test the hypothesis that honeydew excreted by the aphid Eriosoma lanigerum could serve as a trophic resource for its parasitoid Aphelinus mali as well as a kairomone used by the parasitoid to discover its hosts. Results indicate that honeydew increased longevity of A. mali females if water was provided. Water could be necessary to feed on this food source because of its viscosity and its coating by wax. The presence of honeydew allowed longer stinging events by A. mali on E. lanigerum. However, no preference towards honeydew was observed, when given the choice. The role of honeydew excreted by E. lanigerum on A. mali feeding and searching behavior to increase its efficiency as a biological control agent is discussed.

Interactions between Rice Resistance to Planthoppers and Honeydew-Related Egg Parasitism under Varying Levels of Nitrogenous Fertilizer.

Host plant resistance is the most researched method for the management of planthoppers and leafhoppers in tropical rice. For optimal effects, resistance should be resilient to fertilizer inputs and work in synergy with natural enemies. In field plot experiments, we examined how rice resistance and fertilizer inputs affect mortality of planthopper and leafhopper eggs by hymenopteran parasitoids. We used IR62 as a variety with resistance to Nilaparvata lugens (Stål) [BPH], Sogatella furcifera (Horváth) [WBPH] and Nephotettix virescens (Distant) [GLH], and IR64 as a susceptible control. The herbivores were more abundant during wet season sampling in low-nitrogen plots. During this study, parasitoids killed between 31 and 38% of BPH eggs and 24 and 52% of WBPH eggs during four days of field exposure. Parasitism, mainly due to Oligosita spp., was generally higher in high-nitrogen and IR64 plots. Similar densities of eggs in exposed plants suggest that these trends were mediated by semiochemicals and therefore support the Optimal Defense Hypothesis. Honeydew from BPH on IR62 had more xylem-derived wastes than honeydew on IR64. We applied honeydew from both varieties to sentinel plants. Parasitism by Anagrus spp. was higher on plants of either variety treated with honeydew derived from IR62; however, the effect was only apparent in high-nitrogen plots. Results suggest that Anagrus spp., by responding to honeydew, will counter the nitrogen-induced enhancement of planthopper fitness on resistant rice.

Compatibility of Insecticides with Rice Resistance to Planthoppers as Influenced by the Timing and Frequency of Applications.

The brown planthopper, Nilaparvata lugens (Stål)(BPH) is a pest of rice in Asia. We examined the effects of seven insecticides combined with host resistance against BPH. In a screenhouse environment, we treated BPH-infested and non-infested resistant (IR62) and susceptible (IR64) rice with buprofezin, carbofuran, cartap hydrochloride, cypermethrin, deltamethrin, fipronil, or thiamethoxam + chlorantraniliprole. In one experiment, plants received one, two or three applications. In a second experiment, plants received one early or late insecticide application. Carbofuran and fipronil reduced planthopper biomass densities but resistance did not contribute to these effects (i.e., resistance was redundant). Single applications of cartap hydrochloride (at 20 or 50 days after sowing (DAS)), cypermethrin (20 DAS), or buprofezin (50 DAS) reduced BPH biomass densities on IR62 (i.e., synergies); other insecticides and application times, and multiple applications of all insecticides did not reduce BPH biomass densities on IR62 more than on IR64 (i.e., either resistance or insecticides were redundant). Deltamethrin (three applications) was antagonistic to resistance, but host resistance tended to buffer against the negative effects of single deltamethrin applications. Yields of infested IR62 were not statistically improved by insecticide applications. Late applications reduced yields of non-infested rice. We discuss how prophylactic insecticide applications could destabilize BPH populations and reduce the productivity and profitability of resistant rice.

Adaptation by the Brown Planthopper to Resistant Rice: A Test of Female-Derived Virulence and the Role of Yeast-like Symbionts.

The adaptation by planthoppers to feed and develop on resistant rice is a challenge for pest management in Asia. We conducted a series of manipulative experiments with the brown planthopper (Nilaparvata lugens (Stål)) on the resistant rice variety IR62 (BPH3/BPH32 genes) to assess behavioral and bionomic changes in planthoppers exhibiting virulence adaptation. We also examined the potential role of yeast-like symbionts (YLS) in virulence adaptation by assessing progeny fitness (survival × reproduction) following controlled matings between virulent males or females and avirulent males or females, and by manipulating YLS densities in progeny through heat treatment. We found virulence-adapted planthoppers developed faster, grew larger, had adults that survived for longer, had female-biased progeny, and produced more eggs than non-selected planthoppers on the resistant variety. However, feeding capacity-as revealed through honeydew composition-remained inefficient on IR62, even after 20+ generations of exposure to the resistant host. Virulence was derived from both the male and female parents; however, females contributed more than males to progeny virulence. We found that YLS are essential for normal planthopper development and densities are highest in virulent nymphs feeding on the resistant host; however, we found only weak evidence that YLS densities contributed more to virulence. Virulence against IR62 in the brown planthopper, therefore, involves a complex of traits that encompass a series of behavioral, physiological, and genetic mechanisms, some of which are determined only by the female parent.

Changes in reflectance of rice seedlings during planthopper feeding as detected by digital camera: Potential applications for high-throughput phenotyping.

Damage to grasses and cereals by phloem-feeding herbivores is manifest as nutrient and chlorophyll loss, desiccation, and a gradual decline in host vigour. Chlorophyll loss in particular leads to a succession of colour changes before eventual host death. Depending on the attacking herbivore species, colour changes can be difficult to detect with the human eye. This study used digital images to examine colour changes of rice seedlings during feeding by the brown planthopper, Nilaparvata lugens (Stål) and whitebacked planthopper, Sogatella furcifera (Horváth). Values for red (580 nm), green (540 nm) and blue (550 nm) reflectance for 39 rice varieties during seedling seed-box tests were derived from images captured with a digital camera. Red and blue reflectance gradually increased as herbivore damage progressed until final plant death. Red reflectance was greater from plants attacked by the brown planthopper than plants attacked by the whitebacked planthopper, which had proportionately more green and blue reflectance, indicating distinct impacts by the two planthoppers on their hosts. Analysis of digital images was used to discriminate variety responses to the two planthoppers. Ordination methods based on red-green-blue reflectance and vegetation indices such as the Green Leaf Index (GLI) that included blue reflectance were more successful than two-colour indices or indices based on hue, saturation and brightness in discriminating between damage responses among varieties. We make recommendations to advance seed-box screening methods for cereal resistance to phloem feeders and demonstrate how images from digital cameras can be used to improve the quality of data captured during high-throughput phenotyping.

Feeding behavior, life history, and virus transmission ability of Bemisia tabaci Mediterranean species (Hemiptera: Aleyrodidae) under elevated CO2.

The continuous rise of CO2 concentrations in the atmosphere is reducing plant nutritional quality for herbivores and indirectly affects their performance. The whitefly (Bemisia tabaci, Gennadius) is a major worldwide pest of agricultural crops causing significant yield losses. This study investigated the plant-mediated indirect effects of elevated CO2 on the feeding behavior and life history of B. tabaci Mediterranean species. Eggplants were grown under elevated and ambient CO2 concentrations for 3 weeks after which plants were either used to monitor the feeding behavior of whiteflies using the Electrical Penetration Graph technique or to examine fecundity and fertility of whiteflies. Plant leaf carbon, nitrogen, phenols and protein contents were also analyzed for each treatment. Bemisia tabaci feeding on plants exposed to elevated CO2 showed a longer phloem ingestion and greater fertility compared to those exposed to ambient CO2 suggesting that B. tabaci is capable of compensating for the plant nutritional deficit. Additionally, this study looked at the transmission of the virus Tomato yellow leaf curl virus (Begomovirus) by B. tabaci exposing source and receptor tomato plants to ambient or elevated CO2 levels before or after virus transmission tests. Results indicate that B. tabaci transmitted the virus at the same rate independent of the CO2 levels and plant treatment. Therefore, we conclude that B. tabaci Mediterranean species prevails over the difficulties that changes in CO2 concentrations may cause and it is predicted that under future climate change conditions, B. tabaci would continue to be considered a serious threat for agriculture worldwide.

Resistance and tolerance to the brown planthopper, Nilaparvata lugens (Stål), in rice infested at different growth stages across a gradient of nitrogen applications.

High resource availability can reduce anti-herbivore resistance (a plant's ability to defend against herbivores and reduce damage) in rice, Oryza sativa L, but may also increase tolerance (a plant's ability to withstand damage by, for example, compensatory growth). Through a series of greenhouse, screenhouse and field experiments, this study examines fitness (survival and development × reproduction) of the brown planthopper, Nilaparvata lugens (Stål), on resistant (IR62) and susceptible (IR22) rice varieties and age-related rice tolerance to planthopper damage under varying resource (nitrogenous fertilizer) availability. Planthoppers reared on IR62 in the greenhouse had lower fitness than planthoppers on IR22. IR62 became increasingly resistant as plants aged. IR22 was generally more tolerant of planthopper damage, and tolerance increased in IR22, but declined in IR62, as the plants aged. Rice plants infested at pre-tillering stages (3-4 leaf stage) in the screenhouse had greater losses to root, shoot and grain yield per unit weight of planthopper than plants infested at tillering stages, particularly in IR22. These trends were mainly due to the impact of planthoppers during pre-tillering stages and the length of exposure to the planthoppers. High nitrogen compromised IR62 resistance, particularly in tillering plants in the greenhouse study; however, high nitrogen did not increase planthopper biomass-density on IR62 in greenhouse or field cages. Tolerance to damage in IR62 at mid-tillering stages declined under increasing levels of nitrogen, but nitrogen increased tolerance during late-tillering stages. Planthopper damage to IR22 in field cages was severe and hopperburn (plant death) occurred in 83% of IR22 plants under high nitrogen (60-150 kg N ha-1). In contrast, despite planthopper infestations, damage to IR62 was low in field-grown plants and productivity (tillers, roots, shoots and grain) increased in IR62 under increasing nitrogen. Our results indicate that, whereas nitrogenous fertilizer increases planthopper fitness on susceptible and resistant varieties, the net effects of high nitrogen on IR62 include decreased planthopper biomass-density (apparent in all experiments) and higher tolerance to damage during later growth stages (observed in the greenhouse, and during one of two seasons in field cages).

Morphological variation of Aphidius ervi Haliday (Hymenoptera: Braconidae) associated with different aphid hosts.

BACKGROUND: Parasitoids are frequently used in biological control due to the fact that they are considered host specific and highly efficient at attacking their hosts. As they spend a significant part of their life cycle within their hosts, feeding habits and life history of their host can promote specialization via host-race formation (sequential radiation). The specialized host races from different hosts can vary morphologically, behaviorally and genetically. However, these variations are sometimes inconspicuous and require more powerful tools in order to detect variation such as geometric morphometrics analysis. METHODS: We examined Aphidius ervi, an important introduced biological control agent in Chile associated with a great number of aphid species, which are exploiting different plant hosts and habitats. Several combinations (biotypes) of parasitoids with various aphid/host plant combinations were analyzed in order to obtain measures of forewing shape and size. To show the differences among defined biotypes, we chose 13 specific landmarks on each individual parasitoid wing. The analysis of allometric variation calculated in wing shape and size over centroid size (CS), revealed the allometric changes among biotypes collected from different hosts. To show all differences in shape of forewings, we made seven biotype pairs using an outline-based geometric morphometrics comparison. RESULTS: The biotype A. pis_pea (Acyrthosiphon pisum on pea) was the extreme wing size in this study compared to the other analyzed biotypes. Aphid hosts have a significant influence in the morphological differentiation of the parasitoid forewing, splitting biotypes in two groups. The first group consisted of biotypes connected with Acyrthosiphon pisum on legumes, while the second group is composed of biotypes connected with aphids attacking cereals, with the exception of the R. pad_wheat (Rhopalosiphum padi on wheat) biotype. There was no significant effect of plant species on parasitoid wing size and shape. DISCUSSION: Although previous studies have suggested that the genotype of parasitoids is of greater significance for the morphological variations of size and shape of wings, this study indicates that the aphid host on which A. ervi develops is the main factor to alter the structure of parasitoid forewings. Bigger aphid hosts implied longer and broader forewings of A. ervi.