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Insects, Volume 10, Issue 10 (October 2019)

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Cover Story (view full-size image) We investigated community perceptions of a recently-introduced response to codling moth control in [...] Read more.
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Open AccessArticle
Comparative Analysis of Intra- and Inter-Specific Genomic Variability in the Peach Potato Aphid, Myzus persicae
Insects 2019, 10(10), 368; https://doi.org/10.3390/insects10100368 - 22 Oct 2019
Abstract
The availability of genomic data in the last decade relating to different aphid species has allowed the analysis of the genomic variability occurring among such species, whereas intra-specific variability has hitherto very largely been neglected. In order to analyse the intra-genomic [...] Read more.
The availability of genomic data in the last decade relating to different aphid species has allowed the analysis of the genomic variability occurring among such species, whereas intra-specific variability has hitherto very largely been neglected. In order to analyse the intra-genomic variability in the peach potato aphid, Myzus persicae, comparative analyses were performed revealing several clone-specific gene duplications, together with numerous deletions/rearrangements. Our comparative approach also allowed us to evaluate the synteny existing between the two M. persicae clones tested and between the peach potato aphid and the pea aphid, Acyrthosiphon pisum. Even if part of the observed rearrangements are related to a low quality of some assembled contigs and/or to the high number of contigs present in these aphid genomes, our evidence reveals that aphid clones are genetically more different than expected. These results suggest that the choice of performing genomes sequencing combining different biotypes/populations, as revealed in the case of the soybean aphid, Aphis glycines, is unlikely to be very informative in aphids. Interestingly, it is possible that the holocentric nature of aphid chromosomes favours genome rearrangements that can be successively inherited transgenerationally via the aphid’s apomictic (parthenogenetic) mode of reproduction. Lastly, we evaluated the structure of the cluster of genes coding for the five histones (H1, H2A, H2B, H3 and H4) in order to better understand the quality of the two M. persicae genomes and thereby to improve our knowledge of this functionally important gene family. Full article
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Open AccessCommunication
Termite-Induced Injuries to Maize and Baby Corn under Organic and Conventional Farming Systems in the Central Highlands of Kenya
Insects 2019, 10(10), 367; https://doi.org/10.3390/insects10100367 - 22 Oct 2019
Abstract
Termite-induced injuries to maize and baby corn were evaluated in on-going comparison experiments on organic and conventional farming systems at two trial sites in the Central Highlands of Kenya (Chuka and Thika). The farming systems were established in 2007 at two input levels: [...] Read more.
Termite-induced injuries to maize and baby corn were evaluated in on-going comparison experiments on organic and conventional farming systems at two trial sites in the Central Highlands of Kenya (Chuka and Thika). The farming systems were established in 2007 at two input levels: Low input level, representing subsistence farming (Conv-Low, Org-Low) and high input level, representing commercial farming (Conv-High, Org-High). Termite-induced injuries to maize and baby corn, such as tunneling the stem or lodging the whole plant were assessed over two cropping seasons. The lodging occurred exclusively at Thika. It first became apparent in the Org-Low system, with most of lodging occurring during the vegetative stage. Baby corn grown under high input systems showed increasing lodging from the late vegetative crop stage and peaked before the final harvest. Tunneling was recorded at both sites, but was generally below 5%, with no significant differences between the farming systems. Overall, the injury patterns caused by termites appear to be a function of the plant growth stage, termite colony activities, trial site, and the types and levels of fertilizer input. Thus, the management practice used in each farming system (organic or conventional) might have greater influence on crop injuries than the type of farming system itself or the termite abundance within each system. Full article
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Open AccessReview
Honey Bee Alarm Pheromone Mediates Communication in Plant–Pollinator–Predator Interactions
Insects 2019, 10(10), 366; https://doi.org/10.3390/insects10100366 - 21 Oct 2019
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Abstract
Honey bees play a crucial role in pollination, and in performing this critical function, face numerous threats from predators and parasites during foraging and homing trips. Back in the nest, their defensive behavior drives some individuals to sacrifice themselves while fighting intruders with [...] Read more.
Honey bees play a crucial role in pollination, and in performing this critical function, face numerous threats from predators and parasites during foraging and homing trips. Back in the nest, their defensive behavior drives some individuals to sacrifice themselves while fighting intruders with their stingers or mandibles. During these intense conflicts, bees release alarm pheromone to rapidly communicate with other nest mates about the present danger. However, we still know little about why and how alarm pheromone is used in plant–pollinator–predator interactions. Here, we review the history of previously detected bee alarm pheromones and the current state of the chemical analyses. More new components and functions have been confirmed in honey bee alarm pheromone. Then, we ask how important the alarm pheromones are in intra- and/or inter-species communication. Some plants even adopt mimicry systems to attract either the pollinators themselves or their predators for pollination via alarm pheromone. Pheromones are honest signals that evolved in one species and can be one of the main driving factors affecting co-evolution in plant–pollinator–predator interactions. Our review intends to stimulate new studies on the neuronal, molecular, behavioral, and evolutionary levels in order to understand how alarm pheromone mediates communication in plant–pollinator–predator interactions. Full article
(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)
Open AccessArticle
Expansion of Imaginal Disc Growth Factor Gene Family in Diptera Reflects the Evolution of Novel Functions
Insects 2019, 10(10), 365; https://doi.org/10.3390/insects10100365 - 20 Oct 2019
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Abstract
Imaginal disc growth factors (IDGFs) are a small protein family found in insects. They are related to chitinases and implicated in multiple functions, including cell growth stimulation, antimicrobial activity, insect hemolymph clotting, and maintenance of the extracellular matrix. A number of new IDGFs [...] Read more.
Imaginal disc growth factors (IDGFs) are a small protein family found in insects. They are related to chitinases and implicated in multiple functions, including cell growth stimulation, antimicrobial activity, insect hemolymph clotting, and maintenance of the extracellular matrix. A number of new IDGFs have been found in several insect species and their detailed phylogenetic analysis provides a good basis for further functional studies. To achieve this goal, we sequenced Idgf cDNAs from several lepidopteran and trichopteran species and supplemented our data with sequences retrieved from public databases. A comparison of Idgf genes in different species showed that Diptera typically contain several Idgf paralogs with a simple exon-intron structure (2–3 exons), whereas lepidopteran Idgfs appear as a single copy per genome and contain a higher number of exons (around 9). Our results show that, while lepidopteran Idgfs, having single orthologs, are characterized by low divergence and stronger purifying selection over most of the molecule, the duplicated Idgf genes in Diptera, Idgf1 and Idgf4, exhibit signs of positive selection. This characterization of IDGF evolution provides, to our knowledge, the first information on the changes that formed these important molecules. Full article
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Open AccessArticle
Cnaphalocrocis medinalis Moths Decide to Migrate when Suffering Nutrient Shortage on the First Day after Emergence
Insects 2019, 10(10), 364; https://doi.org/10.3390/insects10100364 - 20 Oct 2019
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Abstract
Migration is a costly strategy in terms of reproduction output. Competition for limited internal resources leads to physiological management of migration-reproduction trade-offs in energy allocation. Migratory insects must choose to determine to allocate energy into reproduction or migration when confronted insufficient energy supply. [...] Read more.
Migration is a costly strategy in terms of reproduction output. Competition for limited internal resources leads to physiological management of migration-reproduction trade-offs in energy allocation. Migratory insects must choose to determine to allocate energy into reproduction or migration when confronted insufficient energy supply. Although nutrient shortage is known to stimulate insect migration to escape deteriorating habitat, little is known about when and how migratory insects make decisions when confronted by a nutritional shortage. Here Cnaphalocrocis medinalis (Lepidoptera: Pyralidae), a migratory rice pest in eastern Asia, was used to study the effects of starvation on reproductive traits, behavioral traits and energy allocation. The result showed that one or two days’ starvation before preoviposition did not significantly reduce the fertility (total egg per female laid) and flight capability (flight duration and distance) of both sexes C. medinalis. The preoviposition period was extended significantly only if moths were starved starting on the first day after emergence. Also, take-off percentage of moths starved since their first day increased significantly, and continued to increase even if supplemental nutrients were supplied as honey solution in later days. Moths starved on the first day appeared to allocate or transfer triglycerides into the thorax to maintain the migration process: the quantity of thoracic triglycerides did not differ with age, but abdominal triglycerides decreased with age if starvation continued. These results indicate that the first day post-emergence is a critical period for C. medinalis to decide to migrate or not in response to lack of food. This furthers our understanding of the population dynamics of migratory insects under natural conditions. Full article
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Open AccessArticle
New Method of Analysis of Lipids in Tribolium castaneum (Herbst) and Rhyzopertha dominica (Fabricius) Insects by Direct Immersion Solid-Phase Microextraction (DI-SPME) Coupled with GC–MS
Insects 2019, 10(10), 363; https://doi.org/10.3390/insects10100363 - 19 Oct 2019
Viewed by 202
Abstract
Lipids play an essential role in providing energy and other physiological functions for insects. Therefore, it is important to determine the composition of insect lipids from cuticular and internal tissues for a better understanding of insect biology and physiology. A novel non-derivatization method [...] Read more.
Lipids play an essential role in providing energy and other physiological functions for insects. Therefore, it is important to determine the composition of insect lipids from cuticular and internal tissues for a better understanding of insect biology and physiology. A novel non-derivatization method for the analysis of lipids including fatty acids, hydrocarbon waxes, sterols in Tribolium castaneum (Herbst) and Rhyzopertha dominica (Fabricius) was explored using the direct immersion solid-phase microextraction (DI-SPME) coupled with gas chromatography–mass spectrometry (GC–MS). Nine extraction solvents, acetonitrile, methanol, hexane, ethanol, chloroform, acetonitrile and ethanol (1:1 v/v), acetonitrile and water (1:1 v/v), ethanol and water (1:1 v/v) and acetonitrile and ethanol and water (2:2:1 v/v/v) were selected and evaluated for the extraction of insect lipids with DI-SPME fiber. Acetonitrile extraction offered the best qualitative, quantitative, and number of lipids extracted from insects samples results. Acetonitrile extracted high-boiling point compounds from both species of tested insects. The range of hydrocarbons was C25 (pentacosane) to C32 (dotriacontane) for T. castaneum and C26 (11-methylpentacosane) to C34 (tetratriacontane) for R. dominica. The major compounds extracted from the cuticular surface of T. castaneum were 11-methylheptacosane (20.71%) and 3-methylheptacosane (12.37%), and from R. dominica were 10-methyldotriacontane (14.0%), and 15-methyltritriacontane (9.93%). The limit of detection (LOD) for the n-alkane compounds ranged between 0.08 (nonacosane) and 0.26 (dotriacontane) µg/g and for the fatty acids between 0.65 (arachidic acid) to 0.89 (oleic acid) µg/g. The study indicated that DI-SPME GC–MS is a highly efficient extraction and a sensitive analytical method for the determination of non-derivatized insect lipids in cuticular and homogenized body tissues. Full article
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Open AccessArticle
Ιnteractions between Beauveria bassiana and Isaria fumosorosea and Their Hosts Sitophilus granarius (L.) and Sitophilus oryzae (L.) (Coleoptera: Curculionidae)
Insects 2019, 10(10), 362; https://doi.org/10.3390/insects10100362 - 19 Oct 2019
Viewed by 158
Abstract
The interactions between the entomopathogenic fungus Beauveria bassiana Balsamo (Vuillemin) (Hypocreales: Cordycipitaceae) and the entomopathogenic fungus Isaria fumosorosea (Wize) Brown and Smith (Hypocreales: Clavicipitaceae) were examined on young adults of Sitophilus granarius (L.) (Coleoptera: Curculionidae) and S. oryzae (L.) (Coleoptera: Curculionidae). Conidial suspensions [...] Read more.
The interactions between the entomopathogenic fungus Beauveria bassiana Balsamo (Vuillemin) (Hypocreales: Cordycipitaceae) and the entomopathogenic fungus Isaria fumosorosea (Wize) Brown and Smith (Hypocreales: Clavicipitaceae) were examined on young adults of Sitophilus granarius (L.) (Coleoptera: Curculionidae) and S. oryzae (L.) (Coleoptera: Curculionidae). Conidial suspensions of these entomopathogenic fungi were applied both separately and in combination, at three dosages, 104, 106, and 108 conidia/mL. Mortality of experimental adults was recorded daily for 15 days. An overall positive interaction between the pathogenic microorganisms was observed. Mean weevil mortality caused by the separate acting fungi, B. bassiana, ranged from 26.7% to 53.3% and from 36.6% to 63.3% for S. granarius and S. oryzae, respectively. The respective values for I. fumosorosea were 20.0%–53.3% and 46.7%–66.7%. The combined treatments showed a distinct interaction between the pathogens; for S. granarius, the interaction between the pathogens was additive in all combinations, whereas, for S. oryzae, the interaction was additive in seven and competitive in two of the combinations. Applying both entomopathogenic microorganisms may offer a method for weevil control that could be more effective than using each pathogen alone. Full article
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Open AccessEditorial
Advancing the Science of Tick and Tick-Borne Disease Surveillance in the United States
Insects 2019, 10(10), 361; https://doi.org/10.3390/insects10100361 - 19 Oct 2019
Viewed by 200
Abstract
Globally, vector-borne diseases are an increasing public health burden; in the United States, tick-borne diseases have tripled in the last three years. The United States Centers for Disease Control and Prevention (CDC) recognizes the need for resilience to the increasing vector-borne disease burden [...] Read more.
Globally, vector-borne diseases are an increasing public health burden; in the United States, tick-borne diseases have tripled in the last three years. The United States Centers for Disease Control and Prevention (CDC) recognizes the need for resilience to the increasing vector-borne disease burden and has called for increased partnerships and sustained networks to identify and respond to the most pressing challenges that face vector-borne disease management, including increased surveillance. To increase applied research, develop communities of practice, and enhance workforce development, the CDC has created five regional Centers of Excellence in Vector-borne Disease. These Centers are a partnership of public health agencies, vector control groups, academic institutions, and industries. This special issue on tick and tick-borne disease surveillance is a collection of research articles on multiple aspects of surveillance from authors that are affiliated with or funded by the CDC Centers of Excellence. This body of work illustrates a community-based system of research by which participants share common problems and use integrated methodologies to produce outputs and effect outcomes that benefit human, animal and environmental health. Full article
(This article belongs to the Special Issue Tick Surveillance and Tick-borne Diseases)
Open AccessArticle
Insecticidal Activity of Compounds of Plant Origin on Mahanarva spectabilis (Hemiptera: Cercopidae)
Insects 2019, 10(10), 360; https://doi.org/10.3390/insects10100360 - 19 Oct 2019
Viewed by 94
Abstract
The damage caused by spittlebugs varies according to the species of grass, and the losses can reach alarming levels. Measures for population control are currently restricted to the use of resistant grasses and the diversification of pastures. Therefore, alternative control measures are necessary, [...] Read more.
The damage caused by spittlebugs varies according to the species of grass, and the losses can reach alarming levels. Measures for population control are currently restricted to the use of resistant grasses and the diversification of pastures. Therefore, alternative control measures are necessary, such as the use of botanical insecticides. The aim of this study was to evaluate the insecticidal activities of thymol, carvacrol, eugenol, cinnamaldehyde, and trans-anethole on Mahanarva spectabilis eggs, nymphs, and adults under laboratory conditions. In the egg tests, treatments with eugenol, carvacrol, and thymol showed the highest mortalities, presenting efficiencies higher than 85% after 48 h of application. In the nymph tests, the treatments with thymol and carvacrol at 2.5% and eugenol at 2.0% and 2.5% showed intermediate efficiencies, with values above 61%. The highest mortality was observed in the treatment with trans-anethole at 2.5%, with an efficiency of 95%. In the tests with adults, only treatment with trans-anethole at 2.5% obtained an efficiency reaching 90%; in the other treatments, the efficiency did not exceed 51%. These results showed that, at these concentrations, trans-anethole presents a high rate of insecticidal activity on M. spectabilis nymphs and adults and, therefore, is recommended as a potential natural insecticide for the control of this pest. Full article
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Open AccessArticle
Male Horn Lack of Allometry May be Tied to Food Relocation Behaviour in Lifting Dung Beetles (Coleoptera, Scarabaeidae, Eucraniini)
Insects 2019, 10(10), 359; https://doi.org/10.3390/insects10100359 - 18 Oct 2019
Viewed by 182
Abstract
The small dung beetle tribe Eucraniini includes extremely specialized species that have been defined as “lifters” according to their food relocation behaviour. They are characterized by the presence of well-developed expansions on the head and pronotum, which can be included in the large [...] Read more.
The small dung beetle tribe Eucraniini includes extremely specialized species that have been defined as “lifters” according to their food relocation behaviour. They are characterized by the presence of well-developed expansions on the head and pronotum, which can be included in the large and varied group of horns, whose presence is usually related to complex reproductive tactics. In this study, two closely related species, Anomiopsoides cavifrons and A. heteroclyta, were examined employing traditional and geometric morphometrics to test whether the Eucraniini has polymorphic males that might exhibit different reproductive tactics, as in the sister tribe Phanaeini, for which a male trimorphism was demonstrated. If also present in Eucraniini polyphenism could be considered a plesiomorphy common to the two clades. The inter- and intraspecific shape variation and object symmetry of the head and the scaling relationships between body size and traits were evaluated. Marked interspecific and small intraspecific differences in shape variation, high symmetry, and similar isometric growth patterns were shown in both species. The hypothesis of male polymorphism in Anomiopsoides was thus rejected. Instead, the results supported the alternative hypothesis that Eucraniini lacks male polymorphism, perhaps due to functional constraints affecting the shape of the structures involved in their peculiar food relocating behaviour. Full article
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Open AccessArticle
House Flies (Musca domestica) Pose a Risk of Carriage and Transmission of Bacterial Pathogens Associated with Bovine Respiratory Disease (BRD)
Insects 2019, 10(10), 358; https://doi.org/10.3390/insects10100358 - 18 Oct 2019
Viewed by 179
Abstract
House flies are important nuisance pests in a variety of confined livestock operations. More importantly, house flies are known mechanical vectors of numerous animal and human pathogens. Bovine respiratory disease (BRD) is an economically important, complex illness of cattle associated with several bacteria [...] Read more.
House flies are important nuisance pests in a variety of confined livestock operations. More importantly, house flies are known mechanical vectors of numerous animal and human pathogens. Bovine respiratory disease (BRD) is an economically important, complex illness of cattle associated with several bacteria and viruses. The role of flies in the ecology and transmission of bacterial pathogens associated with BRD is not understood. Using culture-dependent and culture-independent methods, we examined the prevalence of the BRD bacterial complex Mannheimia haemolytica, Pasteurella multocida and Histophilus somni in house flies collected in a commercial feedlot from a pen with cattle exhibiting apparent BRD symptoms. Using both methods, M. haemolytica was detected in 11.7% of house flies, followed by P. multocida (5.0%) and H. somni (3.3%). The presence of BRD bacterial pathogens in house flies suggests that this insect plays a role in the ecology of BRD pathogens and could pose a risk as a potential reservoir and/or a vector of BRD pathogens among individual cattle and in their environment. Full article
(This article belongs to the Special Issue Control of House Flies and Stable Flies)
Open AccessArticle
Ozone Effectiveness on Wheat Weevil Suppression: Preliminary Research
Insects 2019, 10(10), 357; https://doi.org/10.3390/insects10100357 - 18 Oct 2019
Viewed by 188
Abstract
Insect infestations within stored product facilities are a major concern to livestock and human food industries. Insect infestations in storage systems can result in economic losses of up to 20%. Furthermore, the presence of insects and their waste and remains in grain and [...] Read more.
Insect infestations within stored product facilities are a major concern to livestock and human food industries. Insect infestations in storage systems can result in economic losses of up to 20%. Furthermore, the presence of insects and their waste and remains in grain and stored foods may pose a health risk to humans and livestock. At present, pests in commercial storage are managed by a combination of different methods ranging from cleaning and cooling to treatment of the stored material with contact insecticides or fumigation. The availability of pesticides for the treatment of grain and other stored products is decreasing owing, in some cases, to environmental and safety concerns among consumers and society, thus emphasizing the need for alternative eco-friendly pest control methods. One of the potential methods is the use of ozone. Although the mechanism of action of ozone on insects is not completely known, the insect’s respiratory system is a likely the target of this gas. The main goal of this investigation was to determine the efficacy of ozone in the suppression of adult wheat weevils Sitophilus granarius. In the experiments conducted, different durations of ozone exposure were tested. In addition to ozone toxicity, the walking response and velocity of wheat weevils were investigated. The results showed the harmful effects of ozone on these insects. In addition to mortality, ozone also had negative effects on insect speed and mobility. The efficiency of the ozone treatment increased with increasing ozone exposure of insects. The ability of ozone to reduce the walking activity and velocity of treated insects is a positive feature in pest control in storage systems, thereby reducing the possibility of insects escaping from treated objects. The results of this investigation suggest that ozone has the potential to become a realistic choice for suppressing harmful insects in storage systems for humans and livestock, either alone or as a complement to other control methods. Full article
Open AccessReview
Natural Product Medicines for Honey Bees: Perspective and Protocols
Insects 2019, 10(10), 356; https://doi.org/10.3390/insects10100356 - 18 Oct 2019
Viewed by 156
Abstract
The western honey bee remains the most important pollinator for agricultural crops. Disease and stressors threaten honey bee populations and productivity during winter- and summertime, creating costs for beekeepers and negative impacts on agriculture. To combat diseases and improve overall bee health, researchers [...] Read more.
The western honey bee remains the most important pollinator for agricultural crops. Disease and stressors threaten honey bee populations and productivity during winter- and summertime, creating costs for beekeepers and negative impacts on agriculture. To combat diseases and improve overall bee health, researchers are constantly developing honey bee medicines using the tools of microbiology, molecular biology and chemistry. Below, we present a manifesto alongside standardized protocols that outline the development and a systematic approach to test natural products as ‘bee medicines’. These will be accomplished in both artificial rearing conditions and in colonies situated in the field. Output will be scored by gene expression data of host immunity, bee survivorship, reduction in pathogen titers, and more subjective merits of the compound in question. Natural products, some of which are already encountered by bees in the form of plant resins and nectar compounds, provide promising low-cost candidates for safe prophylaxis or treatment of bee diseases. Full article
(This article belongs to the Special Issue Biology of Social Insect Diseases)
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Open AccessArticle
Lethal Effects of High Temperatures on Brown Marmorated Stink Bug Adults before and after Overwintering
Insects 2019, 10(10), 355; https://doi.org/10.3390/insects10100355 - 18 Oct 2019
Viewed by 116
Abstract
The invasive brown marmorated stink bug, Halyomorpha halys, is causing economic and ecological damage in invaded areas. Its overwintering behavior warrants mitigation practices in warehouses and shipping operations. The aim of this study was to characterize the mortality response curves of H. [...] Read more.
The invasive brown marmorated stink bug, Halyomorpha halys, is causing economic and ecological damage in invaded areas. Its overwintering behavior warrants mitigation practices in warehouses and shipping operations. The aim of this study was to characterize the mortality response curves of H. halys adults to short high-temperature exposure. Here we compared field-collected individuals entering (ENA) and exiting diapause (EXA). EXA adults displayed increased susceptibility to high temperatures compared to ENA individuals. Complete mortality of all tested individuals was obtained after 10 min exposure at 50.0 °C, and after 15 (EXA) or 20 min (ENA) at 47.5 °C. The nutritional status of these insects had no effect on high-temperature tolerance. The mortality curves obtained here may be used for the definition of cost-effective heat treatments aimed at the H. halys control. Full article
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Open AccessReview
Effects of the Herbicide Glyphosate on Honey Bee Sensory and Cognitive Abilities: Individual Impairments with Implications for the Hive
Insects 2019, 10(10), 354; https://doi.org/10.3390/insects10100354 - 18 Oct 2019
Viewed by 125
Abstract
The honeybee Apis mellifera is an important pollinator in both undisturbed and agricultural ecosystems. Its great versatility as an experimental model makes it an excellent proxy to evaluate the environmental impact of agrochemicals using current methodologies and procedures in environmental toxicology. The increase [...] Read more.
The honeybee Apis mellifera is an important pollinator in both undisturbed and agricultural ecosystems. Its great versatility as an experimental model makes it an excellent proxy to evaluate the environmental impact of agrochemicals using current methodologies and procedures in environmental toxicology. The increase in agrochemical use, including those that do not target insects directly, can have deleterious effects if carried out indiscriminately. This seems to be the case of the herbicide glyphosate (GLY), the most widely used agrochemical worldwide. Its presence in honey has been reported in samples obtained from different environments. Hence, to understand its current and potential risks for this pollinator it has become essential to not only study the effects on honeybee colonies located in agricultural settings, but also its effects under laboratory conditions. Subtle deleterious effects can be detected using experimental approaches. GLY negatively affects associative learning processes of foragers, cognitive and sensory abilities of young hive bees and promotes delays in brood development. An integrated approach that considers behavior, physiology, and development allows not only to determine the effects of this agrochemical on this eusocial insect from an experimental perspective, but also to infer putative effects in disturbed environments where it is omnipresent. Full article
(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)
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Open AccessArticle
Comparative Microbiome Profiles of Sympatric Tick Species from the Far-Western United States
Insects 2019, 10(10), 353; https://doi.org/10.3390/insects10100353 - 18 Oct 2019
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Abstract
Insight into the composition and function of the tick microbiome has expanded considerably in recent years. Thus far, tick microbiome studies have focused on species and life stages that are responsible for transmitting disease. In this study we conducted extensive field sampling of [...] Read more.
Insight into the composition and function of the tick microbiome has expanded considerably in recent years. Thus far, tick microbiome studies have focused on species and life stages that are responsible for transmitting disease. In this study we conducted extensive field sampling of six tick species in the far-western United States to comparatively examine the microbial composition of sympatric tick species: Ixodes pacificus, Ixodes angustus, Dermacentor variabilis, Dermacentor occidentalis, Dermacentor albipictus, and Haemaphysalis leporispalustris. These species represent both common vectors of disease and species that rarely encounter humans, exhibiting a range of host preferences and natural history. We found significant differences in microbial species diversity and composition by tick species and life stage. The microbiome of most species examined were dominated by a few primary endosymbionts. Across all species, the relative abundance of these endosymbionts increased with life stage while species richness and diversity decreased with development. Only one species, I. angustus, did not show the presence of a single dominant microbial species indicating the unique physiology of this species or its interaction with the surrounding environment. Tick species that specialize in a small number of host species or habitat ranges exhibited lower microbiome diversity, suggesting that exposure to environmental conditions or host blood meal diversity can affect the tick microbiome which in turn may affect pathogen transmission. These findings reveal important associations between ticks and their microbial community and improve our understanding of the function of non-pathogenic microbiomes in tick physiology and pathogen transmission. Full article
(This article belongs to the Special Issue Vectors and Vector-borne Diseases)
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Open AccessArticle
Functional Characterization of Outer Membrane Proteins (OMPs) in Xenorhabdus nematophila and Photorhabdus luminescens through Insect Immune Defense Reactions
Insects 2019, 10(10), 352; https://doi.org/10.3390/insects10100352 - 17 Oct 2019
Viewed by 163
Abstract
Xenorhabdus nematophila and Photorhabdus luminescens are entomopathogenic bacterial symbionts that produce toxic proteins that can interfere with the immune system of insects. Herein, we show that outer membrane proteins (OMPs) could be involved as bacterial virulence factors. Purified totals OMPs of both bacterial [...] Read more.
Xenorhabdus nematophila and Photorhabdus luminescens are entomopathogenic bacterial symbionts that produce toxic proteins that can interfere with the immune system of insects. Herein, we show that outer membrane proteins (OMPs) could be involved as bacterial virulence factors. Purified totals OMPs of both bacterial species were injected into fifth instar larvae of Spodoptera exigua Hübner. Larvae were surveyed for cellular defenses fluctuations in total haemocyte counts (THC) and granulocyte percentage and for the humoral defenses protease, phospholipase A2 (PLA2), and phenoloxidase (PO) activities at specific time intervals. Changes in the expression of the three inducible antimicrobial peptides (AMPs), cecropin, attacin, and spodoptericin, were also measured. Larvae treated with OMPs of both bacterial species had more haemocytes than did the negative controls. OMPs of X. nematophila caused more haemocyte destruction than did the OMPs of P. luminescens. The OMPs of both bacterial species initially activated insect defensive enzymes post-injection, the degree of activation varying with enzyme type. The AMPs, attacin, cecropin, and spodoptericin were up-regulated by OMP injections compared with the normal larvae. The expression of these three AMPs was maximal at four hours post injection (hpi) with P. luminescens OMPs treatment. Expression of the three AMPs in X. nematophila treated insects was irregular and lower than in the P. luminescens OMPs treatment. These findings provide insights into the role of OMPs of entomopathogenic nematode bacterial symbionts in countering the physiological defenses of insects. Full article
(This article belongs to the Special Issue The Insect Response against Entomopathogenic Nematodes)
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Open AccessArticle
Cold Tolerance and Population Dynamics of Leptoglossus zonatus (Hemiptera: Coreidae)
Insects 2019, 10(10), 351; https://doi.org/10.3390/insects10100351 - 17 Oct 2019
Viewed by 127
Abstract
In California’s San Joaquin Valley, feeding by the coreid pest, Leptoglossus zonatus, can cause considerable economic loss on almond and pistachio. This research was conducted to improve understanding of how winter temperatures affect mortality of overwintering adult L. zonatus and to develop [...] Read more.
In California’s San Joaquin Valley, feeding by the coreid pest, Leptoglossus zonatus, can cause considerable economic loss on almond and pistachio. This research was conducted to improve understanding of how winter temperatures affect mortality of overwintering adult L. zonatus and to develop a better understanding of the role pomegranate plays in the species’ life-history. We exposed 7410 field-collected adult L. zonatus to temperatures between −2 and −10 °C for a period of three, four, or six hours using insect incubators. At six hours of exposure, the, LD50 and LD95 occur at −5.8 and −9.7 °C, respectively. We classified L. zonatus as chill-intolerant. Temperatures cold enough to affect substantial mortality of overwintering L. zonatus rarely occur in the San Joaquin Valley. Whole aggregation destructive sampling from a pomegranate hedgerow in Fresno County was conducted to determine population dynamics. At late summer to early fall, aggregations consisted of >90% immature stages. By early to mid-winter, mean aggregation size decreased, consisting of only three to 12 late-instars and adults. During years one and two of the experiment, L. zonatus produced a generation on pomegranate, mostly between September and mid-November. Overwintering did not occur on pomegranate, rather the majority of adults emigrated to other overwintering locations by mid-winter. Full article
(This article belongs to the Special Issue Monitoring and Detection of Insect Resistance)
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Open AccessArticle
A Subset of Odorant Receptors from the Desert Locust Schistocerca gregaria Is Co-Expressed with the Sensory Neuron Membrane Protein 1
Insects 2019, 10(10), 350; https://doi.org/10.3390/insects10100350 - 17 Oct 2019
Viewed by 211
Abstract
In the desert locust Schistocerca gregaria (S. gregaria), pheromones are considered to be crucial for governing important behaviors and processes, including phase transition, reproduction, aggregation and swarm formation. The receptors mediating pheromone detection in olfactory sensory neurons (OSNs) on the antenna [...] Read more.
In the desert locust Schistocerca gregaria (S. gregaria), pheromones are considered to be crucial for governing important behaviors and processes, including phase transition, reproduction, aggregation and swarm formation. The receptors mediating pheromone detection in olfactory sensory neurons (OSNs) on the antenna of S. gregaria are unknown. Since pheromone receptors in other insects belong to the odorant receptor (OR) family and are typically co-expressed with the “sensory neuron membrane protein 1” (SNMP1), in our search for putative pheromone receptors of S. gregaria, we have screened the OR repertoire for receptor types that are expressed in SNMP1-positive OSNs. Based on phylogenetic analyses, we categorized the 119 ORs of S. gregaria into three groups (I–III) and analyzed a substantial number of ORs for co-expression with SNMP1 by two-color fluorescence in situ hybridization. We have identified 33 ORs that were co-expressed with SNMP1. In fact, the majority of ORs from group I and II were found to be expressed in SNMP1-positive OSNs, but only very few receptors from group III, which comprises approximately 60% of all ORs from S. gregaria, were co-expressed with SNMP1. These findings indicate that numerous ORs from group I and II could be important for pheromone communication. Collectively, we have identified a broad range of candidate pheromone receptors in S. gregaria that are not randomly distributed throughout the OR family but rather segregate into phylogenetically distinct receptor clades. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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Open AccessArticle
Analysis of miRNAs in the Heads of Different Castes of the Bumblebee Bombus lantschouensis (Hymenoptera: Apidae)
Insects 2019, 10(10), 349; https://doi.org/10.3390/insects10100349 - 16 Oct 2019
Viewed by 244
Abstract
Bumblebees are important insect pollinators for many wildflowers and crops. MicroRNAs (miRNAs) are endogenous non-coding small RNAs that regulate different biological functions in insects. In this study, the miRNAs in the heads of the three castes of the bumblebee Bombus lantschouensis were identified [...] Read more.
Bumblebees are important insect pollinators for many wildflowers and crops. MicroRNAs (miRNAs) are endogenous non-coding small RNAs that regulate different biological functions in insects. In this study, the miRNAs in the heads of the three castes of the bumblebee Bombus lantschouensis were identified and characterized by small RNA deep sequencing. The significant differences in the expression of miRNAs and their target genes were analyzed. The results showed that the length of the small RNA reads from males, queens, and workers was distributed between 18 and 30 nt, with a peak at 22 nt. A total of 364 known and 89 novel miRNAs were identified from the heads of the three castes. The eight miRNAs with the highest expressed levels in males, queens, and workers were identical, although the order of these miRNAs based on expression differed. The male vs. queen, male vs. worker, and worker vs. queen comparisons identified nine, fourteen, and four miRNAs with significant differences in expression, respectively. The different castes were clustered based on the differentially expressed miRNAs (DE miRNAs), and the expression levels of the DE miRNAs obtained by RT-qPCR were consistent with the read counts obtained through Solexa sequencing. The putative target genes of these DE miRNAs were enriched in 29 Gene Ontology (GO) terms, and catalytic activity was the most enriched GO term, as demonstrated by its association with 2837 target genes in the male vs. queen comparison, 3535 target genes in the male vs. worker comparison, and 2185 target genes in the worker vs. queen comparison. This study highlights the characteristics of the miRNAs in the three B. lantschouensis castes and will aid further studies on the functions of miRNAs in bumblebees. Full article
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Open AccessReview
Genetics in the Honey Bee: Achievements and Prospects toward the Functional Analysis of Molecular and Neural Mechanisms Underlying Social Behaviors
Insects 2019, 10(10), 348; https://doi.org/10.3390/insects10100348 - 16 Oct 2019
Viewed by 237
Abstract
The European honey bee is a model organism for studying social behaviors. Comprehensive analyses focusing on the differential expression profiles of genes between the brains of nurse bees and foragers, or in the mushroom bodies—the brain structure related to learning and memory, and [...] Read more.
The European honey bee is a model organism for studying social behaviors. Comprehensive analyses focusing on the differential expression profiles of genes between the brains of nurse bees and foragers, or in the mushroom bodies—the brain structure related to learning and memory, and multimodal sensory integration—has identified candidate genes related to honey bee behaviors. Despite accumulating knowledge on the expression profiles of genes related to honey bee behaviors, it remains unclear whether these genes actually regulate social behaviors in the honey bee, in part because of the scarcity of genetic manipulation methods available for application to the honey bee. In this review, we describe the genetic methods applied to studies of the honey bee, ranging from classical forward genetics to recently developed gene modification methods using transposon and CRISPR/Cas9. We then discuss future functional analyses using these genetic methods targeting genes identified by the preceding research. Because no particular genes or neurons unique to social insects have been found yet, further exploration of candidate genes/neurons correlated with sociality through comprehensive analyses of mushroom bodies in the aculeate species can provide intriguing targets for functional analyses, as well as insight into the molecular and neural bases underlying social behaviors. Full article
(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)
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Open AccessArticle
Temperature and Sugar Feeding Effects on the Activity of a Laboratory Strain of Aedes aegypti
Insects 2019, 10(10), 347; https://doi.org/10.3390/insects10100347 - 16 Oct 2019
Viewed by 239
Abstract
Aedes aegypti is an invasive mosquito species that is expected to expand its global distribution through climate change. As poikilotherms, mosquitoes are greatly affected by the temperature of the environment which can impact host-seeking, blood-feeding, and flight activity as well as survival and [...] Read more.
Aedes aegypti is an invasive mosquito species that is expected to expand its global distribution through climate change. As poikilotherms, mosquitoes are greatly affected by the temperature of the environment which can impact host-seeking, blood-feeding, and flight activity as well as survival and ability to transmit pathogens. However, an important aspect of mosquito biology on which the effect of temperature has not been investigated is water and sugar-feeding and how access to a sugar source might affect the insect’s activity and survival under different thermal conditions. To close this knowledge gap, we relied on actometer experiments to study the activity of both female and male Ae. aegypti at 20 °C, 25 °C, and 30 °C, providing either water or 10% sucrose to the insects. We then measured the total carbohydrate contents of alive mosquitoes using the anthrone protocol. Survival was assessed and compared between all groups. Results from this study will inform on the thermal biology of Ae. aegypti mosquitoes and how access to sugar affects their activity. Full article
(This article belongs to the Special Issue Vectors and Vector-borne Diseases)
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Open AccessArticle
Variation in an Extreme Weapon: Horn Performance Differences across Rhinoceros Beetle (Trypoxylus dichotomus) Populations
Insects 2019, 10(10), 346; https://doi.org/10.3390/insects10100346 - 15 Oct 2019
Viewed by 169
Abstract
Japanese rhinoceros beetle (Trypoxylus dichotomus) males have exaggerated head horns that they use as weapons in combat over reproductive opportunities. In these contests, there is an advantage to having a longer horn, and there seems to be little cost to horn [...] Read more.
Japanese rhinoceros beetle (Trypoxylus dichotomus) males have exaggerated head horns that they use as weapons in combat over reproductive opportunities. In these contests, there is an advantage to having a longer horn, and there seems to be little cost to horn exaggeration. However, populations vary in the amount of horn exaggeration across this widespread species. Here, we examine four populations and quantify scaling and functional morphology of the horn. We then measure force production by the horn system in a combat-relevant movement. We find that not only does horn length vary among populations, but allometry of lever mechanics and force production varies in a complex way. For instance, some beetle populations make relatively long horns, but exert relatively low forces. Other populations make shorter horns and produce higher forces during fights. We suggest that this performance variation could be associated with differences in the intensity or type of sexual selection across the species. Full article
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Open AccessArticle
Sulfoxaflor Applied via Drip Irrigation Effectively Controls Cotton Aphid (Aphis gossypii Glover)
Insects 2019, 10(10), 345; https://doi.org/10.3390/insects10100345 - 14 Oct 2019
Viewed by 195
Abstract
Aphis gossypii Glover is a major pest of cotton and can severely affect cotton yield and lint quality. In this study, the efficacy of sulfoxaflor applied via drip irrigation and foliar spray on controlling cotton aphids was evaluated in 2016 and 2017 in [...] Read more.
Aphis gossypii Glover is a major pest of cotton and can severely affect cotton yield and lint quality. In this study, the efficacy of sulfoxaflor applied via drip irrigation and foliar spray on controlling cotton aphids was evaluated in 2016 and 2017 in Xinjiang, China. The distribution of sulfoxaflor in cotton roots, stems, leaves, and aphids, as well as its effects on two natural enemies of aphids, were also investigated. Results showed that sulfoxaflor applied through drip irrigation mainly concentrated in leaves and provided effective control of cotton aphids for 40 days, compared to 20 days when applied through foliar spray. Furthermore, drip application resulted in much lower sulfoxaflor concentrations in aphids than foliar spray. As a result, ladybird beetle and lacewing populations were higher in drip applied plants than in foliar sprayed plants. Additionally, the cost of drip irrigation was lower than foliar spray as cotton plants are commonly irrigated via drip irrigation in Xinjiang. Our results showed that application of sulfoxaflor through drip irrigation is an effective way of controlling cotton aphids in Xinjiang due to a prolonged control period, safety to two natural enemies, and lower cost of application. Full article
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Open AccessReview
The Neurophysiological Bases of the Impact of Neonicotinoid Pesticides on the Behaviour of Honeybees
Insects 2019, 10(10), 344; https://doi.org/10.3390/insects10100344 - 14 Oct 2019
Viewed by 231
Abstract
Acetylcholine is the main excitatory neurotransmitter in the honeybee brain and controls a wide range of behaviours that ensure the survival of the individuals and of the entire colony. Neonicotinoid pesticides target this neurotransmission pathway and can thereby affect the behaviours under its [...] Read more.
Acetylcholine is the main excitatory neurotransmitter in the honeybee brain and controls a wide range of behaviours that ensure the survival of the individuals and of the entire colony. Neonicotinoid pesticides target this neurotransmission pathway and can thereby affect the behaviours under its control, even at doses far below the toxicity limit. These sublethal effects of neonicotinoids on honeybee behaviours were suggested to be partly responsible for the decline in honeybee populations. However, the neural mechanisms by which neonicotinoids influence single behaviours are still unclear. This is mainly due to the heterogeneity of the exposure pathways, doses and durations between studies. Here, we provide a review of the state of the science in this field and highlight knowledge gaps that need to be closed. We describe the agonistic effects of neonicotinoids on neurons expressing the different nicotinic acetylcholine receptors and the resulting brain structural and functional changes, which are likely responsible for the behavioural alterations reported in bees exposed to neonicotinoids. Full article
(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)
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Open AccessArticle
Survival and Development of Striacosta albicosta (Smith) (Lepidoptera: Noctuidae) Immature Stages on Dry Beans, non-Bt, Cry1F, and Vip3A Maize
Insects 2019, 10(10), 343; https://doi.org/10.3390/insects10100343 - 13 Oct 2019
Viewed by 266
Abstract
Striacosta albicosta is a crop pest that causes economic damage in the United States and Canada. Only maize and dry beans are shown to be suitable hosts, since larval development is incomplete on other hosts. The objective of this study was to describe [...] Read more.
Striacosta albicosta is a crop pest that causes economic damage in the United States and Canada. Only maize and dry beans are shown to be suitable hosts, since larval development is incomplete on other hosts. The objective of this study was to describe the developmental parameters of immature stages of S. albicosta feeding on dry beans, non-Bt, Cry1F, and Vip3A maize. For Vip3A, mortality was 100% after 24 h. Larvae feeding on non-Bt maize had the highest larval survival (70.6%) compared to the other hosts. Maize expressing Cry1F had higher survival (31.3%) than dry beans (26.0%). Larvae feeding on dry beans had a significantly faster total development time (74.8 days), compared to 92.5 days for non-Bt and 96.2 days for Cry1F. All larvae developed through seven instars. Pupae from larvae that had fed on non-Bt maize were significantly heavier than pupae from other hosts. An understanding of S. albicosta immature development on various host plants is needed to improve recommendations for effective scouting, treatment timing, and economic thresholds. Differential development can result in an extended adult emergence period, and possibly result in assortative mating between Bt susceptible and resistant populations, which violates the assumption of random mating necessary for current resistance management strategies for Bt maize. Therefore, understanding the impact of host plant and transgenic traits on aspects of pest biology will aid in developing effective integrated pest management and insect resistance management strategies for this pest. Full article
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Open AccessReview
The Role of Landscapes and Landmarks in Bee Navigation: A Review
Insects 2019, 10(10), 342; https://doi.org/10.3390/insects10100342 - 12 Oct 2019
Viewed by 181
Abstract
The ability of animals to explore landmarks in their environment is essential to their fitness. Landmarks are widely recognized to play a key role in navigation by providing information in multiple sensory modalities. However, what is a landmark? We propose that animals use [...] Read more.
The ability of animals to explore landmarks in their environment is essential to their fitness. Landmarks are widely recognized to play a key role in navigation by providing information in multiple sensory modalities. However, what is a landmark? We propose that animals use a hierarchy of information based upon its utility and salience when an animal is in a given motivational state. Focusing on honeybees, we suggest that foragers choose landmarks based upon their relative uniqueness, conspicuousness, stability, and context. We also propose that it is useful to distinguish between landmarks that provide sensory input that changes (“near”) or does not change (“far”) as the receiver uses these landmarks to navigate. However, we recognize that this distinction occurs on a continuum and is not a clear-cut dichotomy. We review the rich literature on landmarks, focusing on recent studies that have illuminated our understanding of the kinds of information that bees use, how they use it, potential mechanisms, and future research directions. Full article
(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)
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Open AccessReview
Microbial Control of Invasive Forest Pests with Entomopathogenic Fungi: A Review of the Current Situation
Insects 2019, 10(10), 341; https://doi.org/10.3390/insects10100341 - 12 Oct 2019
Viewed by 223
Abstract
The health of the forestlands of the world is impacted by a number of insect pests and some of them cause significant damage with serious economic and environmental implications. Whether it is damage of the North American cypress aphid in South America and [...] Read more.
The health of the forestlands of the world is impacted by a number of insect pests and some of them cause significant damage with serious economic and environmental implications. Whether it is damage of the North American cypress aphid in South America and Africa, or the destruction of maple trees in North America by the Asian long horned beetle, invasive forest pests are a major problem in many parts of the world. Several studies explored microbial control opportunities of invasive forest pests with entomopathogenic bacteria, fungi, and viruses, and some are successfully utilized as a part of integrated forest pest management programs around the world. This manuscript discusses some invasive pests and the status of their microbial control around the world with entomopathogenic fungi. Full article
(This article belongs to the Special Issue Ecology and Management of Forest Insects in a Changing World)
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Open AccessArticle
Sub-Lethal Doses of Clothianidin Inhibit the Conditioning and Biosensory Abilities of the Western Honeybee Apis mellifera
Insects 2019, 10(10), 340; https://doi.org/10.3390/insects10100340 - 11 Oct 2019
Viewed by 226
Abstract
Insects play an important role in the stability of ecosystems by fulfilling key functions such as pollination and nutrient cycling, as well as acting as prey for amphibians, reptiles, birds and mammals. The global decline of insects is therefore a cause for concern, [...] Read more.
Insects play an important role in the stability of ecosystems by fulfilling key functions such as pollination and nutrient cycling, as well as acting as prey for amphibians, reptiles, birds and mammals. The global decline of insects is therefore a cause for concern, and the role of chemical pesticides must be examined carefully. The lethal effects of insecticides are well understood, but sub-lethal concentrations have not been studied in sufficient detail. We therefore used the western honeybee Apis mellifera as a model to test the effect of the neonicotinoid insecticide clothianidin on the movement, biosensory abilities and odor-dependent conditioning of insects, titrating from lethal to sub-lethal doses. Bees treated with sub-lethal doses showed no significant movement impairment compared to untreated control bees, but their ability to react to an aversive stimulus was inhibited. These results show that clothianidin is not only highly toxic to honeybees, but can, at lower doses, also disrupt the biosensory capabilities of survivors, probably reducing fitness at the individual level. In our study, sub-lethal doses of clothianidin altered the biosensory abilities of the honeybee; possible consequences at the colony level are discussed. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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Open AccessArticle
Identification of Regulatory Host Genes Involved in Sigma Virus Replication Using RNAi Knockdown in Drosophila
Insects 2019, 10(10), 339; https://doi.org/10.3390/insects10100339 - 11 Oct 2019
Viewed by 233
Abstract
The Drosophila melanogaster sigma virus, a member of the Rhabdoviridae family, specifically propagates itself in D. melanogaster. It contains six genes in the order of 3′-NPXMGL-5′. The sigma virus is [...] Read more.
The Drosophila melanogaster sigma virus, a member of the Rhabdoviridae family, specifically propagates itself in D. melanogaster. It contains six genes in the order of 3′-NPXMGL-5′. The sigma virus is the only arthropod-specific virus of the Rhabdoviridae family. Sigma-virus-infected Drosophila may suffer from irreversible paralysis when exposed to a high CO2 concentration, but generally, no other symptoms are reported. A recent study reported that host gene expression in immune pathways was not changed in sigma-virus-infected Drosophila, which does not necessarily suggest that they are not involved in virus–host interactions. The present study aimed to identify host genes associated with sigma virus replication. Immune pathways JAK-STAT and IMD were selected for detailed study. The results showed that the genome copy number of the sigma virus increased after knocking down the immune pathway genes domeless and PGRP-LC in Drosophila S2 cells. The knocking down of domeless and PGRP-LC significantly up-regulated the expression of the L gene compared to the other viral genes. We propose that the immune pathways respond to sigma virus infection by altering L expression, hence suppressing viral replication. This effect was further tested in vivo, when D. melanogaster individuals injected with dsdome and dsPGRP-LC showed not only an increase in sigma virus copy number, but also a reduced survival rate when treated with CO2. Our study proved that host immunity influences viral replication, even in persistent infection. Knocking down the key components of the immune process deactivates immune controls, thus facilitating viral expression and replication. We propose that the immunity system of D. melanogaster regulates the replication of the sigma virus by affecting the L gene expression. Studies have shown minimal host–virus interaction in persistent infection. However, our study demonstrated that the immunity continued to affect viral replication even in persistent infection because knocking down the key components of the immune process disabled the relevant immune controls and facilitated viral expression and replication. Full article
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