High promiscuity among females of the invasive pest species Drosophila suzukii.

Drosophila suzukii (Matsumura, 1931), the spotted-wing drosophila, is a highly invasive fruit fly that spread from Southern Asia across most regions of Asia and, in the last 15 years, has invaded Europe and the Americas. It is an economically important pest of small fruits such as berries and stone fruits. Drosophila suzukii speciated by adapting to cooler, mountainous, and forest environments. In temperate regions, it evolved seasonal polyphenism traits which enhanced its survival during stressful winter population bottlenecks. Consequently, in these temperate regions, the populations undergo seasonal reproductive dynamics. Despite its economic importance, no data are available on the behavioural reproductive strategies of this fly. The presence of polyandry, for example, has not been determined despite the important role it might play in the reproductive dynamics of populations. We explored the presence of polyandry in an established population in Trentino, a region in northern Italy. In this area, D. suzukii overcomes the winter bottleneck and undergoes a seasonal reproductive fluctuation. We observed a high remating frequency in females during the late spring demographic explosion that led to the abundant summer population. The presence of a high degree of polyandry and shared paternity associated with the post-winter population increase raises the question of the possible evolutionary adaptive role of this reproductive behaviour in D. suzukii.

Distinct and Temporally Stable Assembly Mechanisms Shape Bacterial and Fungal Communities in Vineyard Soils.

Microbial communities in agricultural soils are fundamental for plant growth and in vineyard ecosystems contribute to defining regional wine quality. Managing soil microbes towards beneficial outcomes requires knowledge of how community assembly processes vary across taxonomic groups, spatial scales, and through time. However, our understanding of microbial assembly remains limited. To quantify the contributions of stochastic and deterministic processes to bacterial and fungal assembly across spatial scales and through time, we used 16 s rRNA gene and ITS sequencing in the soil of an emblematic wine-growing region of Italy.Combining null- and neutral-modelling, we found that assembly processes were consistent through time, but bacteria and fungi were governed by different processes. At the within-vineyard scale, deterministic selection and homogenising dispersal dominated bacterial assembly, while neither selection nor dispersal had clear influence over fungal assembly. At the among-vineyard scale, the influence of dispersal limitation increased for both taxonomic groups, but its contribution was much larger for fungal communities. These null-model-based inferences were supported by neutral modelling, which estimated a dispersal rate almost two orders-of-magnitude lower for fungi than bacteria.This indicates that while stochastic processes are important for fungal assembly, bacteria were more influenced by deterministic selection imposed by the biotic and/or abiotic environment. Managing microbes in vineyard soils could thus benefit from strategies that account for dispersal limitation of fungi and the importance of environmental conditions for bacteria. Our results are consistent with theoretical expectations whereby larger individual size and smaller populations can lead to higher levels of stochasticity.

Tissue age, orchard location and disease management influence the composition of fungal and bacterial communities present on the bark of apple trees.

Plants host microbial communities that can be affected by environmental conditions and agronomic practices. Despite the role of bark as a reservoir of plant pathogens and beneficial microorganisms, no information is available on the effects of disease management on the taxonomic composition of the bark-associated communities of apple trees. We assessed the impact of disease management strategies on fungal and bacterial communities on the bark of a scab-resistant apple cultivar in two orchard locations and for two consecutive seasons. The amplicon sequencing revealed that bark age and orchard location strongly affected fungal and bacterial diversity. Microbiota dissimilarity between orchards evolved during the growing season and showed specific temporal series for fungal and bacterial populations in old and young bark. Disease management did not induce global changes in the microbial populations across locations and seasons, but specifically affected the abundance of some taxa according to bark age, orchard location and sampling time. Therefore, the disease management applied to scab-resistant cultivars, which is based on a limited use of fungicides, partially changed the taxonomic composition of bark-associated fungal and bacterial communities, suggesting the need for a more accurate risk assessment regarding possible pathogen outbreaks.

Entomological Opportunities and Challenges for Sustainable Viticulture in a Global Market.

Viticulture has experienced dramatic global growth in acreage and value. As the international exchange of goods has increased, so too has the market demand for sustainably produced products. Both elements redefine the entomological challenges posed to viticulture and have stimulated significant advances in arthropod pest control programs. Vineyard managers on all continents are increasingly combating invasive species, resulting in the adoption of novel insecticides, semiochemicals, and molecular tools to support sustainable viticulture. At the local level, vineyard management practices consider factors such as the surrounding natural ecosystem, risk to fish populations, and air quality. Coordinated multinational responses to pest invasion have been highly effective and have, for example, resulted in eradication of the moth Lobesia botrana from California vineyards, a pest found in 2009 and eradicated by 2016. At the global level, the shared pests and solutions for their suppression will play an increasing role in delivering internationally sensitive pest management programs that respond to invasive pests, climate change, novel vector and pathogen relationships, and pesticide restrictions.

Semiochemical Strategies for Tortricid Moth Control in Apple Orchards and Vineyards in Italy.

- This review summarizes work done in Italy in taking semiochemical-based management of orchard and vineyard pests from the research and development stage to successful commercial deployment. Mating disruption (MD) of codling moth Cydia pomonella (CM) was originally introduced into the Trentino-South Tyrol areas to address the development of CM resistance to insecticides, particularly insect growth regulators (IGRs), and to mitigate the conflict at the rural/urban interface related to the extensive use of insecticides. Although the mountainous terrain of the area was not optimal for the efficacy of MD, commitment and determination led to the rapid adoption of MD technology throughout the region. Grower cooperatives and their field consultants were strongly influential in convincing growers to accept MD technology. Public research institutions conducted extensive research and education, and provided credible assessments of various MD technologies. By 2016, the deployment of MD in effective area-wide strategies in apple (22,100 ha) and grapes (10,450 ha), has resulted in better control of tortricid moth pests and a substantial decrease in insecticide use. Collaboration between the research community and the pheromone industry has resulted in the development of increasingly effective single-species dispensers, as well as multi-species dispensers for the control of both target and secondary pests. Over the last 20 years, hand-applied reservoir dispensers have shown excellent efficacy in both apple and grapes. Recently, aerosol dispensing systems have been shown to be effective in apple orchards. Further research is needed on the efficacy of aerosols in vineyards before the technology can be widely adopted. The successful implementation of MD in apple and grape production in Trentino-South Tyrol is expediting adoption of the technology in other Italian fruit production regions.

Impact of landscape composition on honey bee pollen contamination by pesticides: A multi-residue analysis.

The honey bee is the most common and important managed pollinator of crops. In recent years, honey bee colonies faced high mortality for multiple causes, including land-use change and the use of plant protection products (hereafter pesticides). This work aimed to explore how contamination by pesticides of pollen collected by honey bees was modulated by landscape composition and seasonality. We placed two honey bee colonies in 13 locations in Northern Italy in contrasting landscapes, from which we collected pollen samples monthly during the whole flowering season in 2019 and 2020. We searched for almost 400 compounds, including fungicides, herbicides, insecticides, and acaricides. We then calculated for each pollen sample the Pollen Hazard Quotient (PHQ), an index that provides a measure of multi-residue toxicity of contaminated pollen. Almost all pollen samples were contaminated by at least one compound. We detected 97 compounds, mainly fungicides, but insecticides and acaricides showed the highest toxicity. Fifteen % of the pollen samples had medium-high or high levels of PHQ, which could pose serious threats to honey bees. Fungicides showed a nearly constant PHQ throughout the season, while herbicides and insecticides and acaricides showed higher PHQ values in spring and early summer. Also, PHQ increased with increasing cover of agricultural and urban areas from April to July, while it was low and independent of landscape composition at the end of the season. The cover of perennial crops, i.e., fruit trees and vineyards, but not of annual crops, increased PHQ of pollen samples. Our work highlighted that the potential toxicity of pollen collected by honey bees was modulated by complex interactions among pesticide category, seasonality, and landscape composition. Due to the large number of compounds detected, our study should be complemented with additional experimental research on the potential interactive effects of multiple compounds on honey bee health.

Bridging biotremology and chemical ecology: a new terminology.

Living organisms use both chemical and mechanical stimuli to survive in their environment. Substrate-borne vibrations play a significant role in mediating behaviors in animals and inducing physiological responses in plants, leading to the emergence of the discipline of biotremology. Biotremology is experiencing rapid growth both in fundamental research and in applications like pest control, drawing attention from diverse audiences. As parallels with concepts and approaches in chemical ecology emerge, there is a pressing need for a shared standardized vocabulary in the area of overlap for mutual understanding. In this article, we propose an updated set of terms in biotremology rooted in chemical ecology, using the suffix '-done' derived from the classic Greek word 'δονέω' (pronounced 'doneo'), meaning 'to shake'.

Orientus ishidae (Hemiptera: Cicadellidae): Biology, Direct Damage and Preliminary Studies on Apple Proliferation Infection in Apple Orchard.

The mosaic leafhopper, Orientus ishidae (Matsumura), is an Asian species widespread in Europe that can cause leaf damage in wild trees and transmit disease phytoplasmas to grapevines. Following an O. ishidae outbreak reported in 2019 in an apple orchard in northern Italy, the biology and damage caused by this species to apples were investigated during 2020 and 2021. Our studies included observations on the O. ishidae life cycle, leaf symptoms associated to its trophic activity, and its capability to acquire "Candidatus Phytoplasma mali," a causal agent of Apple Proliferation (AP). The results indicate that O. ishidae can complete the life cycle on apple trees. Nymphs emerged between May and June, and adults were present from early July to late October, with the peak of flight between July and early August. Semi-field observations allowed for an accurate description of leaf symptoms that appeared as a distinct yellowing after a one-day exposure. In field experiments, 23% of the leaves were found damaged. In addition, 16-18% of the collected leafhoppers were found carrying AP phytoplasma. We conclude that O. ishidae has the potential to be a new apple tree pest. However, further studies are required to better understand the economic impact of the infestations.

Factors influencing short-term parasitoid establishment and efficacy for the biological control of Halyomorpha halys with the samurai wasp Trissolcus japonicus.

BACKGROUND: Classical biological control has been identified as the most promising approach to limit the impact of the invasive pest species Halyomorpha halys (Heteroptera: Pentatomidae). This study investigated the parasitism rate at sites where the biocontrol agent Trissolcus japonicus (Hymenoptera: Scelionidae) was released and where its unintentional introduction took place, in the Trentino-South Tyrol region. The effect of land-use composition was studied to understand which factors favor the establishment of hosts and parasitoids, including native and exotic species. RESULTS: The released T. japonicus were detected a year after the start of the program, with a significant parasitoid impact and discovery, compared to control sites. Trissolcus japonicus was the most abundant H. halys parasitoid, and Trissolcus mitsukurii and Anastatus bifasciatus were recorded also. The efficacy of T. mitsukurii was lower in sites where T. japonicus was successfully established, suggesting a possible competitive interaction. Parasitism level by T. japonicus at the release sites was 12.5% in 2020 and 16.4% in 2021. The combined effect of predation and parasitization increased H. halys mortality up to 50% at the release sites. Landscape composition analysis showed that both H. halys and T. japonicus were more likely to be found at sites with lower altitude and with permanent crops, whereas other hosts and parasitoids preferred different conditions. CONCLUSION: Trissolcus japonicus showed a promising impact on H. halys, at release and adventive sites, with minor nontarget effects, mediated by landscape heterogeneity. The prevalence of T. japonicus in landscapes with permanent crops could support IPM in the future. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Combining Irradiation and Biological Control against Brown Marmorated Stink Bug: Are Sterile Eggs a Suitable Substrate for the Egg Parasitoid Trissolcus japonicus?

The brown marmorated stink bug (BMSB), Halyomorpha halys, is a phytophagous invasive pest native to south-eastern Asia, and it is now distributed worldwide. This species is considered to be one of the most damaging insect pests in North America and in Europe. In agriculture, the predominant approach to managing BMSB is based on the use of insecticides, specifically pyrethroids and neonicotinoids. Unfortunately, the biology of the species and its facility to develop mechanisms of resistance to available pesticides has induced farmers and scientists to develop different, least-toxic, and more effective strategies of control. In a territorial area-wide approach, the use of a classical biological control program in combination with other least-toxic strategies has been given prominent consideration. Following exploratory surveys in the native range, attention has focused on Trissolcus japonicus, a small scelionid egg parasitoid wasp that is able to oviposit and complete its larval development in a single egg of H. halys. A common method for detecting egg parasitoids in the native range involves the placement of so-called 'sentinel' egg masses of the pest in the environment for a short period, which are then returned to the laboratory to determine if any of them are parasitized. Outside of the area of origin, the use of fertile sentinel eggs of the alien species may lead to the further release of the pest species; an alternative is to use sterile sentinel eggs to record the presence of new indigenous egg parasitoids or to detect the dispersal of alien species (in this case, T. japonicus) released in a new environment to control the target insect pest species. This study evaluated the performance of three types of sterile sentinel eggs as a suitable substrate for the oviposition and larval development of the egg parasitoid T. japonicus in a context of combining classical biological control with a Sterile Insect Technique (SIT) approach.

Effects of Irradiation on Biology and Mating Behaviour of Wild Males of Brown Marmorated Stink Bug Using a 6 MV Medical Linear Accelerator.

The brown marmorated stink bug, Halyomorpha halys, is a pentatomid bug of Eastern Asian origin that became an economically relevant pest in the Eurasian and American continents. Management of this species is limited to use of chemical insecticides: an inefficient method due to the strong adaptability of the target pest. The sterile insect technique (SIT) is potentially a valid tactic in the search for nontoxic alternatives. In this work, we investigated the suitability of mass-trapped overwintering males, collected during the aggregation phase before the winter diapause, for their release as competitive sterile males in an SIT programme. Differently from previous studies, irradiation was applied with a linear accelerator device that produced high-energy photons. Following a similar scientific protocol with newly emerged irradiated males, the effects of X-ray irradiation on physiological parameters (longevity, fecundity and fertility) were assessed. In addition, behavioural bioassays were carried out in no-choice conditions to evaluate if irradiation interferes with mating processes. The results are very encouraging; the effects of the irradiation at 32 Gy did not differ from the controls in the longevity or fecundity of the exposed overwintering adults. The hatching rate of the eggs laid by the fertile females that had mated with the irradiated males was less than 5%. The results of behavioural bioassays showed that the irradiation did not cause a significant impact on the quality of the sterile males. More research is warranted to evaluate the mating competitiveness of sterile males in semi-field and field conditions.

Electrophysiologically Determined Spectral Responses in Lobesia botrana (Lepidoptera: Tortricidae).

Electrophysiological methods were used to test the visual sensitivity of European grapevine moth, Lobesia botrana (Lepidoptera: Tortricidae) to wavelengths ranging from 300 to 700 nm. For male and females tested, a main, peak response occurred in the 460-540 nm range (blue-green wavelengths) with females having a generally lower response to wavelengths in that range. A second smaller peak was observed for both sexes at the 340-420 nm range. A general linear model indicated that males, virgin females, and mated females did not react differently to changes in wavelength. No moths showed any obvious sensitivity to wavelengths between 580 and 700 nm. Based on our retinal recording data we suggest that UV light traps (≤480 nm) could be utilized alongside pheromone traps when monitoring L. botrana in high risk areas.

Oviposition response of the moth Lobesia botrana to sensory cues from a host plant.

The grapevine moth Lobesia botrana is a generalist insect herbivore and grapevine is one of its hosts. Previous studies have shown that insects use their olfactory abilities to locate hosts from a distance; whereas contact chemoreception mediates the stimulation of oviposition after landing. Little is known about the role of olfaction and its interactions with contact chemoreception and vision once the insect lands on the plant. Plant volatile compounds can be sensed by host-searching insects located some distance from the plant and insects sense both volatile and nonvolatile cues after landing on a plant. In the present study, we investigated the effects of these volatile and nonvolatile cues on the oviposition behavior of L. botrana. A behavioral bioassay with choice was developed in which insects were offered each sensory cue either alone or in combination with one or 2 other cues. Females were allowed to choose between a device with the stimulus and a blank device. Results were evaluated in terms of 2 parameters: quantity of eggs laid (egg counts) and preference for the stimulus (ODI: oviposition discrimination index). Our results suggest that olfaction significantly affects egg quantity and that there is significant synergism between olfaction and vision, in terms of their combined effect on egg quantity. In terms of preference (ODI), our results did not show a significant preference for any single cue; the highest ODI was measured for the full-cue stimulus (olfaction, vision, and contact). For ODI, a significant interaction was observed between olfaction and vision and a nearly significant interaction was observed between the olfactory and contact cues. The results are discussed in relation to the effects of plant sensory cues on the oviposition behavior of L. botrana.

Population genomics of Drosophila suzukii reveal longitudinal population structure and signals of migrations in and out of the continental United States.

Drosophila suzukii, or spotted-wing drosophila, is now an established pest in many parts of the world, causing significant damage to numerous fruit crop industries. Native to East Asia, D. suzukii infestations started in the United States a decade ago, occupying a wide range of climates. To better understand invasion ecology of this pest, knowledge of past migration events, population structure, and genetic diversity is needed. In this study, we sequenced whole genomes of 237 individual flies collected across the continental United States, as well as several sites in Europe, Brazil, and Asia, to identify and analyze hundreds of thousands of genetic markers. We observed strong population structure between Western and Eastern US populations, but no evidence of any population structure between different latitudes within the continental United States, suggesting that there are no broad-scale adaptations occurring in response to differences in winter climates. We detect admixture from Hawaii to the Western United States and from the Eastern United States to Europe, in agreement with previously identified introduction routes inferred from microsatellite analysis. We also detect potential signals of admixture from the Western United States back to Asia, which could have important implications for shipping and quarantine policies for exported agriculture. We anticipate this large genomic dataset will spur future research into the genomic adaptations underlying D. suzukii pest activity and development of novel control methods for this agricultural pest.

Drosophila suzukii (Diptera: Drosophilidae): A Decade of Research Towards a Sustainable Integrated Pest Management Program.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) also known as spotted-wing drosophila (SWD), is a pest native to Southeast Asia. In the last few decades, the pest has expanded its range to affect all major European and American fruit production regions. SWD is a highly adaptive insect that is able to disperse, survive, and flourish under a range of environmental conditions. Infestation by SWD generates both direct and indirect economic impacts through yield losses, shorter shelf life of infested fruit, and increased production costs. Fresh markets, frozen berries, and fruit export programs have been impacted by the pest due to zero tolerance for fruit infestation. As SWD control programs rely heavily on insecticides, exceedance of maximum residue levels (MRLs) has also resulted in crop rejections. The economic impact of SWD has been particularly severe for organic operations, mainly due to the limited availability of effective insecticides. Integrated pest management (IPM) of SWD could significantly reduce chemical inputs but would require substantial changes to horticultural management practices. This review evaluates the most promising methods studied as part of an IPM strategy against SWD across the world. For each of the considered techniques, the effectiveness, impact, sustainability, and stage of development are discussed.

Attraction of female grapevine moth to common and specific olfactory cues from 2 host plants.

In herbivorous insects with more than 1 host plant, attraction to host odor could conceptually be mediated by common compounds, by specific compounds released by each plant or by combinations of common and specific compounds. We have compared the attraction of female grapevine moth, Lobesia botrana, with specific and common (shared) odors from 2 different plants: a wild host (Daphne gnidium) and a recently colonized host (Vitis vinifera). Odor blends eliciting female attraction to V. vinifera have previously been identified. In this study, olfactory cues from D. gnidium were identified by electroantennographic detection and chemical analysis. The attraction of mated females to synthetic odor blends was then tested in a wind tunnel bioassay. Female attraction was elicited by a blend of compounds released by both from D. gnidium and V. vinifera and by 2 blends with the compounds released specifically from each host. However, more complete odor blends of the 2 plants elicited stronger attraction. The common compounds in combination with the specific compounds of D. gnidium were the most attractive blend. This blend was tested with the common compounds presented both in the ratio emitted by D. gnidium and by V. vinifera, but there was no difference in female attraction. Our findings suggest that specific as well as common plant odor cues play a role in L. botrana host recognition and that there is plasticity in attraction to partial blends. The results are discussed in relation to mechanisms behind host odor recognition and the evolution of insect-plant associations.

A study of the effects of 'Candidatus Phytoplasma mali' on the psyllid Cacopsylla melanoneura (Hemiptera: Psyllidae).

Cacopsylla melanoneura is a univoltine psyllid vector of 'Candidatus Phytoplasma mali', the etiological agent of apple proliferation (AP), a severe disease in European apple orchards. The influence of 'Ca. P. mali' on the fitness of C. melanoneura was studied. In the spring of 2007, male-female pairs of field-collected adults were exposed to 'Ca. P. mali'-infected or healthy 'Golden Delicious' apple shoots. Exposure to these diseased shoots did not affect the life span of the adult psyllids. However, significantly fewer eggs were laid on the diseased shoots. Furthermore, fewer of the eggs that were laid on the infected plants hatched. Data suggest a detrimental effect of AP phytoplasma on the fitness of C. melanoneura.

First Report of Leptopilina japonica in Europe.

Drosophila suzukii (Matsumura; Diptera: Drosophilidae) is a key pest of sweet cherry and small fruits worldwide. Biological control remains unutilized in the framework of D. suzukii management. Nonetheless, natural enemies may play an important role in regulating this pest. We report for the first time the presence of Leptopilina japonica Novkovic and Kimura (Hymenoptera: Figitidae) in Europe. Two specimens emerged from ripened fruits and one was collected after direct observation on a cherry tree in June 2019. They showed the distinctive morphological traits already described and shared more than 99% sequence similarity with specimens of L. japonica collected in Asia. This first finding was confirmed by a wider survey carried out in 2020; L. japonica emerged from cherry fruit samples collected in five other sites across the Trentino region, suggesting that L. japonica has already colonized a wide area. Detection of this Asian species is relevant to the future direction in managing D. suzukii, both in Europe and North America. In fact, L. japonica showed similarity with Ganaspis brasiliensis (Ihering) (Hymenoptera: Figitidae), the most promising candidate for the classical biological control, in terms of developmental time, egg maturation, host age preference and lifetime fecundity.

Substrate-Borne Vibrational Communication in the Vector of Apple Proliferation Disease Cacopsylla picta (Hemiptera: Psyllidae).

Cacopsylla picta (Förster, 1848) (Hemiptera: Pysllidae) is the main vector of apple proliferation, a phytoplasma-caused disease. It represents one of the most severe problems in apple orchards, and therefore, there is a mandatory requirement to chemically treat against this pest in the European Union. Sexual communication using substrate-borne vibrations was demonstrated in several psyllid species. Here, we report the characteristics of the vibrational signals emitted by C. picta during courtship behavior. The pair formation process can be divided into two main phases: identification and courtship. Females initiate the communication on the host plant by emitting trains of vibrational pulses and, during courtship, if males reply, by emitting a signal consisting of a series of pre-pulses and a 'buzz', a duet is established. Moreover, a scanning electron microscopy investigation showed the presence of a stridulatory structure on the thorax and wings of both sexes, whereas the video recordings elucidated associated wing movement. The results provide new information about the biology of this phytoplasma vector and could form a basis of an environmentally friendly pest management strategy.

Essential Oils as Post-Harvest Crop Protectants against the Fruit Fly Drosophila suzukii: Bioactivity and Organoleptic Profile.

The essential oils extracted from mandarin (Citrus reticulata Blanco) fruits, and from tea tree (Maleleuca alternifolia (Maiden and Betche) Cheel) leaves have been chemically analyzed and tested for their bioactivity against D. suzukii. Besides, to estimate consumers' acceptability of the essential oil (EO) treatments, we evaluated their impact on the organoleptic characteristics of the EO-treated fruits. The main chemical constituents of the two EOs were 1,8-cineole and 4-terpineol for M. alternifolia (22.4% and 17.6% of the total components, respectively), and limonene (83.6% of the total components) for C. reticulata. The behavioral tests indicate that the two EOs are able to deter D. suzukii oviposition and that D. suzukii shows positive chemotaxis to low concentrations of the EOs and negative chemotaxis when the EO concentration increases. While no negative effects on the organoleptic profiles were detected for fruits treated with C. reticulata EO, the olfactory profile of fruits treated with M. alternifolia EO was so negative that they were defined as "not suitable for consumption" by panellists. Overall, our findings indicate that the use of EOs for the post-harvest protection of small fruits is feasible, provided that the essential oils are selected not only for their bioactivity against the insect pest but also for their affinity with the consumers' sensorial system.