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.

Genome Assembly and Population Sequencing Reveal Three Populations and Signatures of Insecticide Resistance of Tuta absoluta in Latin America.

Tuta absoluta is one of the largest threats to tomato agriculture worldwide. Native to South America, it has rapidly spread throughout Europe, Africa, and Asia over the past two decades. To understand how T. absoluta has been so successful and to improve containment strategies, high-quality genomic resources and an understanding of population history are critical. Here, we describe a highly contiguous annotated genome assembly, as well as a genome-wide population analysis of samples collected across Latin America. The new genome assembly has an L50 of 17 with only 132 contigs. Based on hundreds of thousands of single nucleotide polymorphisms, we detect three major population clusters in Latin America with some evidence of admixture along the Andes Mountain range. Based on coalescent simulations, we find these clusters diverged from each other tens of thousands of generations ago prior to domestication of tomatoes. We further identify several genomic loci with patterns consistent with positive selection and that are related to insecticide resistance, immunity, and metabolism. This data will further future research toward genetic control strategies and inform future containment policies.

Few indirect effects of baculovirus on parasitoids demonstrate high compatibility of biocontrol methods against Tuta absoluta.

BACKGROUND: Combining different biocontrol agents, particularly micro- and macroorganisms, can contribute to new and sustainable pest control approaches. Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is one of the most destructive pests of solanaceous crops. An emerging management strategy consists of biological control using microbial insecticides such as baculoviruses, but with limited efficacy. Thanks to their high target specificity, baculoviruses can be used simultaneously with natural enemies such as parasitoids for improved control of T. absoluta. However, potential indirect nontarget effects of baculoviruses on parasitoids can result from overlapping resource requirements. We assessed whether ovipositing parasitoid females discriminated against virus-treated hosts and examined the outcome of within-host competition between the hymenopteran parasitoids Necremnus tutae (Reuter) (Eulophidae) and Dolichogenidea gelechiidivoris Marsch (Braconidae), and the Phthorimaea operculella granulovirus (PhopGV, Baculoviridae) that infects T. absoluta larvae. RESULTS: Female D. gelechiidivoris discriminated against virus-treated hosts, whereas N. tutae did not. We found few indirect virus-related effects depending on the species, the sex, and the time of virus treatment. Effects were ambivalent for D. gelechiidivoris offspring and ranged from increased male longevity when infection occurred before parasitization to reduced emergence and male longevity when infection occurred after parasitization. N. tutae offspring showed a longer development time and shorter male longevity when they developed in virus-treated hosts. CONCLUSION: The virus had a low impact on parasitoid offspring. In rare cases, adverse effects were detected; however, the low magnitude of these effects is unlikely to reduce the fitness of parasitoid offspring, therefore both parasitoids seem compatible with the baculovirus for control of T. absoluta. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Nonreproductive effects are more important than reproductive effects in a host feeding parasitoid.

When female host feeding parasitoids encounter a potential host, they face a complicated trade-off between either laying an egg for investing in current reproduction or feeding on or killing the host for future reproduction. Few studies have measured these behavioral shift patterns in a given host-parasitoid association thus far. We systematically assessed the behavioral shifts and life history traits of a host feeding parasitoid, Necremnus tutae, on different instars of its host Tuta absoluta. N. tutae females, as idiobiont host feeding parasitoids, can act on the 1st-4th instar larvae of T. absoluta by either host feeding, parasitizing or host killing. Moreover, a significant behavioral shift was observed on different instar hosts. N. tutae preferred to feed on the young hosts (1st and 2nd instars), lay eggs on middle-aged hosts (3rd instars) and kill old hosts (4th instars) by ovipositor-mediated stinging. The offspring of N. tutae showed a significant female-biased sex ratio, with the number of instars of T. absoluta larvae that were parasitized increasing. Specifically, nonreproductive host mortality induced by host feeding and host killing accounted for high percentages of the total mortality (ranging from 70% on 3rd instar hosts to 88% on 1st instar and 4th instar hosts). We hypothesize that N. tutae could be not merely a parasitoid but also a predator. Our results shed light on the nonreproductive abilities of a host feeding parasitoid that should be given further attention, especially when evaluating the efficacy of parasitoids.

Similar Bacterial Communities among Different Populations of a Newly Emerging Invasive Species, Tuta absoluta (Meyrick).

Microorganisms in the guts of insects enhance the adaptability of their hosts with different lifestyles, or those that live in different habitats. Tuta absoluta is an invasive pest that is a serious threat to tomato production in China. It has quickly spread and colonized Xinjiang, Yunnan and other provinces and regions. We used Illumina HiSeq next generation sequencing of the 16S rRNA gene to study and analyze the composition and diversity of the gut microbiota of three geographical populations of T. absoluta. At the phylum level, the most common bacteria in T. absoluta across all three geographical populations were Proteobacteria and Firmicutes. An uncultured bacterium in the Enterobacteriaceae was the dominant bacterial genus in the T. absoluta gut microbiotas. There were no significant differences in alpha diversity metrics among the Spanish, Yunnan and Xinjiang populations. The structures of the gut microbiota of the three populations were similar based on PCoA and NMDS results. The results confirmed that the microbial structures of T. absoluta from different regions were similar.

The Pupal Parasitoid Trichopria drosophilae Is Attracted to the Same Yeast Volatiles as Its Adult Host.

There is increasing evidence that microorganisms, particularly fungi and bacteria, emit volatile compounds that mediate the foraging behaviour of insects and therefore have the potential to affect key ecological relationships. However, to what extent microbial volatiles affect the olfactory response of insects across different trophic levels remains unclear. Adult parasitoids use a variety of chemical stimuli to locate potential hosts, including those emitted by the host's habitat, the host itself, and microorganisms associated with the host. Given the great capacity of parasitoids to utilize and learn odours to increase foraging success, parasitoids of eggs, larvae, or pupae may respond to the same volatiles the adult stage of their hosts use when locating their resources, but compelling evidence is still scarce. In this study, using Saccharomyces cerevisiae we show that Trichopria drosophilae, a pupal parasitoid of Drosophila species, is attracted to the same yeast volatiles as their hosts in the adult stage, i.e. acetate esters. Parasitoids significantly preferred the odour of S. cerevisiae over the blank medium in a Y-tube olfactometer. Deletion of the yeast ATF1 gene, encoding a key acetate ester synthase, decreased attraction of T. drosophilae, while the addition of synthetic acetate esters to the fermentation medium restored parasitoid attraction. Bioassays with individual compounds revealed that the esters alone were not as attractive as the volatile blend of S. cerevisiae, suggesting that other volatile compounds also contribute to the attraction of T. drosophilae. Altogether, our results indicate that pupal parasitoids respond to the same volatiles as the adult stage of their hosts, which may aid them in locating oviposition sites.

Selection of insectary plants for the conservation of biological control agents of aphids and thrips in fruit orchards.

This study evaluated the potential of flowering plant species naturally occurring to promote the conservation and early establishment of key natural enemies of aphids and thrips in apple and peach orchards. Flowering plants present in the North East of Spain, a main fruit production area in Europe, were sampled to determine their flowering period and to identify potential natural enemies present on each plant species. Thirty-six plant species were found blooming from early March to late May and provided an array of flowers that might ensure food resources for natural enemies. Among them, six species - Eruca vesicaria (L.) Cav., Cardaria draba (L.) Desv., Euphorbia serrata (L.) S.G. Gmel., Malva sylvestris L., Anacyclus clavatus (Desf.) Pers. and Diplotaxis erucoides (L.) DC. - hosted a high diversity of potential natural enemies of aphids and thrips. Their blooming started early in the season and lasted for several sampling weeks and they were widely distributed. Moreover, they had available nectar even in those species with protected nectaries. Therefore, these plant species can be considered as promising candidates for inclusion in the ecological infrastructure designed for fruit orchards in the study area to promote the conservation of the biological control agents of aphids and thrips.

Can Insectary Plants Enhance the Presence of Natural Enemies of the Green Peach Aphid (Hemiptera: Aphididae) in Mediterranean Peach Orchards?

Conservation biological control could be an alternative to insecticides for the management of the aphid Myzus persicae (Sulzer). To develop sustainable strategies for M. persicae control in peach orchards in the Mediterranean, a 2-yr field experiment was conducted to identify the key predators of the aphid; to determine whether the proximity of insectary plants boost natural enemies of M. persicae in comparison to the resident vegetation; and whether selected insectary plants enhance natural enemy populations in the margins of peach orchards. Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae) and Episyrphus balteatus De Geer (Diptera: Syrphidae) were the most abundant predators found among sentinel aphid colonies, accounting for 57% and 26%, respectively. Samplings during 2015 yielded twice as many hoverflies in M. persicae sentinel plants close to the insectary plants as those close to the resident vegetation. The abundance of other natural enemies in sentinel plants, depending on their proximity to the insectary plants, was not significantly different in either of the 2 yr. Hoverflies hovered more often over the insectary plants than over the resident vegetation and landed significantly more often on Lobularia maritima (L.) Desv., Moricandia arvensis (L.) DC., and Sinapis alba L. (Brassicales: Brassicaceae) than on Achillea millefollium L. (Asterales: Compositae). Parasitoids were significantly more abundant in L. maritima and A. millefollium. The vicinity of selected insectary plants to peach orchards could improve the presence of hoverflies, which might benefit the biological control of M. persicae.

Resolving the Taxonomic Status of Potential Biocontrol Agents Belonging to the Neglected Genus Lipolexis Förster (Hymenoptera, Braconidae, Aphidiinae) with Descriptions of Six New Species.

Lipolexis is a small genus in the subfamily Aphidiinae represented by one species in Europe (Lipolexis gracilis Förster) and by four in Asia (Lipolexis wuyiensis Chen, L. oregmae Gahan, L. myzakkaiae Pramanik and Raychaudhuri and L. pseudoscutellaris Pramanik and Raychaudhuri). Although L. oregmae is employed in biological control programs against pest aphids, the last morphological study on the genus was completed over 50 years ago. This study employs an integrative approach (morphology and molecular analysis (COI barcode region)), to examine Lipolexis specimens that were sampled worldwide, including specimens from BOLD database. These results establish that two currently recognized species of Lipolexis (L. gracilis, L. oregmae) are actually a species complex and also reveal phylogenetic relationships within the genus. Six new species are described and a global key for the identification of Lipolexis species is provided.

Tuta absoluta (Lepidoptera: Gelechiidae) Success on Common Solanaceous Species from California Tomato Production Areas.

Tuta absoluta (Meyrick) is a devastating pest of tomato that has invaded many regions of the world. To date, it has not been detected in North America, but the pest reached Costa Rica in 2014 and seriously threatens the southern, southwestern, and western United States including California. Although the primary host of T. absoluta is tomato, several other species of Solanaceae may serve as alternative hosts. In our study, we aimed to assess the potential risk that other solanaceous crops and wild species that are often present in and around California tomato fields could serve as hosts. To accomplish this, we conducted greenhouse and laboratory studies to determine whether two common cultivars of fresh market tomato, two common cultivars of tomatillo, and the wild plants, Solanum nigrum L., Solanum sarrachoides (Sendtner), and Datura stramonium L., are suitable hosts for reproduction and development of the pest. According to our results, D. stramonium and tomatillo were unable to sustain T. absoluta larval development in either greenhouse studies or laboratory studies, and therefore, they are not likely to contribute to T. absoluta establishment during an invasion. On the contrary, the two other solanaceous weeds, S. nigrum and S. sarrachoides, share a similar potential as tomato to be reproductive and developmental hosts of T. absoluta, and might play an important role in the establishment of the pest in California.

The Contribution of Surrounding Margins in the Promotion of Natural Enemies in Mediterranean Apple Orchards.

(1) Habitat management can enhance beneficial arthropod populations and provide ecosystem services such as biological control. However, the implementation of ecological infrastructures inside orchards has a number of practical limitations. Therefore, planting/growing insectary plants in the margins of orchards should be considered as an alternative approach. (2) Here, we assessed the efficacy of a flower margin composed by four insectary plant species (Achillea millefolium, Lobularia maritima, Moricandia arvensis and Sinapis alba), which was placed on an edge of four Mediterranean apple orchards to attract natural enemies of two apple tree aphids (Dysaphis plantaginea and Eriosoma lanigerum). We also characterized the natural enemies present in the aphid colonies. (3) Our results show that the implementation of a flower margin at the edge of apple orchards attracts predators (Syrphidae, Thysanoptera, Araneae, Heteroptera, Coleoptera) and parasitoids. Parasitoids are the main natural enemies present in aphid colonies in our area. (4) The implementation of the flower margins successfully recruited natural enemy populations, and the presence of parasitoids in the surroundings of the orchards increased the parasitism of D. plantaginea colonies.

Hymenoptera Complex Associated with Myzus persicae and Hyalopterus spp. in Peach Orchards in Northeastern Spain and Prospects for Biological Control of Aphids.

Aphids are a serious pest for peach crops. They have traditionally been managed with insecticides, but there is increasing concern about the risk that insecticides pose to both humans and the environment. As a first step to use biological control in aphid management, we conducted a 3-year field survey in northeastern Spain to determine which parasitoids and hyperparasitoids were most prevalent on two aphids, Myzus persicae (Sulzer) and Hyalopterus spp. Koch, the most harmful to peach trees. We collected 11 parasitoid species from M. persicae, with Aphidius matricariae (Haliday) being the most abundant. Two parasitoid species were also collected from Hyalopterus spp., Aphidius transcaspicus Telenga and Praon volucre (Haliday). Hyperparasitoid species overlapped between these aphids but their relative abundances differed. We also discuss the possible impacts of hyperparasitoids on parasitoid populations. Our results suggest that it would be feasible to implement biocontrol methods for aphids in integrated pest management programmes in peach orchards. There are a number of primary parasitoid species associated with these aphids, and the nearby crops and wild vegetation in the vicinity and within the orchards may provide a suitable habitat for them. Additionally, some of them are commercially available and might be usable in augmentative releases.

Attraction of Aphidius ervi (Hymenoptera: Braconidae) and Aphidoletes aphidimyza (Diptera: Cecidomyiidae) to Sweet Alyssum and Assessment of Plant Resources Effects on their Fitness.

The green peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) is one of the most economically important aphid species affecting crops worldwide. Since many natural enemies of this aphid have been recorded, biological control of this pest might be a viable alternative to manage it. Selected plant species in field margins might help to provide the natural enemies with food sources to enhance their fitness. This study aimed to investigate if sweet alyssum, Lobularia maritima (L.) (Brassicaceae), is a potential food source for the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) and the predator Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), and whether this flower could contribute to enhance the biological control of M. persicae. Volatiles produced by alyssum, with and without flowers, attracted both natural enemies. This attractiveness to alyssum flowers was disrupted when compared with peach shoots recently infested with a relatively low number of aphids. When aphids were absent, parasitoids exposed to alyssum survived longer than those that fed on a sugar solution or on water. In the case of the predator, alyssum flowers did not benefit longevity since the nectaries were inaccessible to females. However, our results provide evidence that A. aphidimyza would be able to feed on nectar if accessible. The floral resource did not improve the reproductive capacity of the two natural enemies, but the 10% sugar solution increased the egg load of the predator. Provision of other sugar resources, such as flowers with exposed nectaries and extra floral nectar may also be a viable option to improve the biological control of M. persicae.

Nuclear and cytoplasmic differentiation among Mediterranean populations of Bemisia tabaci: testing the biological relevance of cytotypes.

BACKGROUND: The taxonomy of the species complex Bemisia tabaci is still an unresolved issue. Recently, phylogenetic analysis based on mtCOI identified 31 cryptic species. However, mitochondrial diversity is observed within these species, associated with distinct symbiotic bacterial communities forming associations, which here are called cytotypes. The authors investigated the biological significance of two cytotypes (Q1 and Q2) belonging to the Mediterranean species, which have only been found in allopatry in the Western Mediterranean to date. Sampling was done over a few years in Western Europe, and sympatric situations were found that allowed their reproductive compatibility to be tested in the field with the use of microsatellites. RESULTS: The field survey indicated that, in spite of its recent introduction, Q2 is well established in France and Spain, where it coexists with Q1. Microsatellite data showed that, in allopatry, Q1 and Q2 are highly differentiated, while there is little or no genetic differentiation when they coexist in sympatry, suggesting a high rate of hybridisation. Crossing experiments in the lab confirmed their interfertility. CONCLUSION: Q1 and Q2 hybridise, which confirms that they belong to the same species, in spite of the high degree of genetic differentiation at both the cytoplasmic and nuclear levels, and also suggests that their symbiotic bacteria do not prevent hybridisation.

Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin.

Since its detection in the Mediterranean basin at the end of 2006 and later in other European countries, the South American tomato pinworm, Tuta absoluta (Meyrick), has become a serious threat to tomato crops. In newly infested areas, it is especially problematic during the first years of its presence. Nevertheless, after 2-3 years, the incidence of T. absoluta has become less severe in certain areas. There are several factors contributing to this decline, such as the increase in growers' knowledge of pest behaviour and biology and the correct application of integrated pest control strategies. The impact of opportunistic native natural enemies (fortuitous biological control) should be considered as one of the key factors in this decline. In this review, available information on indigenous natural enemies is updated, and the current pest management approaches used against T. absoluta are addressed. Finally, future scenarios for biological control of this pest are discussed.

Within-plant distribution and sampling of single and mixed infestations of Bemisia tabaci and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) in winter tomato crops.

In several areas of Spain, the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and the sweet potato whitefly, Bemisia tabaci (Gennadius), coexist in tomato, Lycopersicon esculentum Miller. For integrated pest management decision-making, it is important to know the abundance of each species, because they exhibit different abilities to transmit viruses, are susceptible to different biological control agents, and have different responses to insecticides. This study was conducted to provide information on the vertical distribution of T. vaporariorumn and B. tabaci in tomato plants grown in greenhouses in winter and to determine the optimal sampling unit and the sample size for estimating egg and nymphal densities of both whitefly species. Eggs of T. vaporariorum were mainly located on the top stratum of the plant, whereas B. tabaci eggs were mainly found on the middle stratum. Nymphs of both species mainly concentrated in the bottom stratum of the plant. When pest abundance and low relative variation were considered, the bottom stratum was selected as the most convenient for sampling nymphs of both whitefly species. Conversely, the same two criteria indicated that either the top or the middle strata could be used when sampling T. vaporariorum and B. tabaci eggs. Several different sampling units were compared to optimize the estimation of nymphal and egg densities in terms of cost efficiency. One disk (1.15 cm in diameter) per leaflet collected from the top stratum of the tomato plant was the most efficient sampling unit for simultaneously estimating the egg densities of the two whitefly species.