The immune response of the whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) when parasitized by Eretmocerus eremicus (Hymenoptera: Aphelinidae).

In insects, the innate immune system is subdivided into cellular and humoral defenses. When parasitoids attack insects, both reactions can be activated and notably, the phenoloxidase (PO) cascade and lytic activity are part of both cellular and humoral defenses. However, to our knowledge, no study has characterized any immune response of the whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) to the attack of Eretmocerus eremicus (Hymenoptera: Aphelinidae). Therefore, the first objective of the present study was to determine whether whitefly nymphs recently parasitized by E. eremicus exhibit any immune response. For this, we estimate the level of prophenoloxidase (proPO), phenoloxidase (PO), and lytic activity by colorimetric assays. A second objective was to assess whether the observed whitefly immune response could be related to a previously reported preference of the predator Geocoris punctipes (Hemiptera: Lygaeidae) for non-parasitized nymphs. We therefore offered non-parasitized and recently parasitized nymphs to the predator. Our results show that parasitism of whitefly nymphs by E. eremicus induced a highly estimated level of proPO and PO, and a lower level of lytic activity. In addition, we found that G. punctipes did not show a preference for non-parasitized over recently parasitized nymphs. The nymphs of T. vaporariorum activated the PO pathway against E. eremicus; however, the increase in proPO and PO levels was traded-off with decreased lytic activity. In addition, the previously reported preference for non-parasitized nymphs was not seen in our experiments, indicating that the induced immune response did not affect predator behavior by G. punctipes.

Influence of the number of hosts and the risk of predation on the foraging behavior of the parasitoid Eretmocerus eremicus.

BACKGROUND: Parasitoids are natural enemies that can modify their behaviors as they search for hosts based on the characteristics of the sites in which they forage. Theoretical models predict that a parasitoid will stay for longer periods in high-quality sites or patches than in those of low quality. In turn, patch quality may be linked to factors such as the number of hosts and the risk of predation. In the present study, we sought to determine if the factors of the number of hosts, risk of predation, and their interaction influence the foraging behavior of the parasitoid Eretmocerus eremicus (Hymenoptera: Aphelinidae) as theory predicts. To do this, we evaluated different parameters of parasitoid foraging behavior, such as residence time, number of oviposition events, and attacks, in sites of different patch quality. RESULTS: Our results show that when the factors, number of hosts, and, risk of predation, were evaluated separately, E. eremicus resided for longer periods and oviposited more frequently in patches with a high number of hosts and low risk of predation than in other patches. However, when both of these factors were combined, only the number of hosts influenced some aspects of the foraging behavior of this parasitoid, such as the number of oviposition events and attacks. CONCLUSION: For some parasitoids like E. eremicus, theoretical predictions may be fulfilled when patch quality is linked to the number of hosts but will not be fully satisfied when patch quality is related to the risk of predation. Furthermore, at sites with different combinations of host numbers and risk of predation, host number appears to be more critical than predation risk. These results suggest that the performance of the parasitoid E. eremicus to control whiteflies will be mainly mediated by the levels of whitefly infestation and, to a small extent, by the risk of predation to which the parasitoid is subjected. © 2023 Society of Chemical Industry.

Systemic whitefly-induced metabolic responses in newly developed distal leaves of husk tomato plants (Physalis philadelphica) impairs whiteflies development.

BACKGROUND: Metabolic reconfiguration in plants is a hallmark response to insect herbivory that occurs in the attack site and systemically in undamaged tissues. Metabolomic systemic responses can occur rapidly while the herbivore is still present and may persist in newly developed tissue to counterattack future herbivore attacks. This study analyzed the metabolic profile of local and newly developed distal (systemic) leaves of husk tomato (Physalis philadelphica) plants after whitefly Trialeurodes vaporariorum infestation. In addition, the effect of these metabolomic adjustments on whitefly oviposition and development was evaluated. RESULTS: Our results indicate that T. vaporariorum infestation induced significant changes in husk tomato metabolic profiles, not only locally in infested leaves, but also systemically in distal leaves that developed after infestation. The distinctive metabolic profile produced in newly developed leaves affected whitefly nymphal development but did not affect female oviposition, suggesting that changes driven by whitefly herbivory persist in the young leaves that developed after the infestation event to avoid future herbivore attacks. CONCLUSIONS: This report contributes to further understanding the plant responses to sucking insects by describing the metabolic reconfiguration in newly developed, undamaged systemic leaf tissues of husk tomato plants after whitefly infestation. © 2022 Society of Chemical Industry.

The Fitness of Mass Rearing Food on the Establishment of Chrysopa pallens in a Banker Plant System under Fluctuating Temperature Conditions.

Banker plant systems can be used to sustain a reproducing population of biological control agents (BCAs) within a crop, thus providing long-term pest suppression. The founder population of natural enemies in banker plant systems is usually mass-reared on factitious hosts. Thus, a better understanding of the population fitness and pest control performance of mass-reared BCAs in the field is crucial when developing integrated pest management (IPM) strategies. In this study, we determined the fitness of the generalist predator, Chrysopa pallens (Hemiptera: Chrysopidae) ever cultured on different food sources (i.e., mass rearing food, Corcyra cephalonica eggs, and aphid food, Megoura japonica) preying on Aphis craccivora in a banker plant system in a greenhouse based on Chi's age-stage, two-sex life table analysis method. The life tables and predation rate parameters of C. pallens were not significantly different between both treatments under fluctuating temperature conditions. Corcyracephalonica eggs did not significantly weaken the performances of C. pallens in a Vicia faba-A. craccivora banker plant system compared to aphids. In conclusion, C. cephalonica eggs can be used for the mass production of C. pallens as the founder population in a banker plant system. Moreover, linking the life table data with the predation rate is an effective strategy for evaluating mass rearing programs in establishing banker plant systems.

Combination of generalist predators, Nesidiocoris tenuis and Macrolophus pygmaeus, with a companion plant, Sesamum indicum: What benefit for biological control of Tuta absoluta?

Tuta absoluta is one of the most damaging pests of tomato crops worldwide. Damage due to larvae may cause up to 100% loss of tomato production. Use of natural enemies to control the pest, notably predatory mirids such as Nesidiocoris tenuis and Macrolophus pygmaeus, is increasingly being promoted. However, considering the potential damage caused to tomatoes by these omnivorous predators in the absence of T. absoluta, an alternative solution could be required to reduce tomato damage and improve the predators' performance. The use of companion plants can be an innovative solution to cope with these issues. The present study aimed to determine the influence of companion plants and alternative preys on the predators' performance in controlling T. absoluta and protecting tomato plants. We evaluated the effect of predators (alone or combined) and a companion plant (sesame (Sesamum indicum)) on T. absoluta egg predation and crop damage caused by N. tenuis. The influence of an alternative prey (Ephestia kuehniella eggs) on the spatial distribution of predators was also evaluated by caging them in the prey presence or absence, either on tomato or sesame plants or on both. We found that the presence of sesame did not reduce the efficacy of N. tenuis or M. pygmaeus in consuming T. absoluta eggs; hatched egg proportion decreased when N. tenuis, M. pygmaeus, or both predators were present. More specifically, this proportion was more strongly reduced when both predators were combined. Sesame presence also reduced necrotic rings caused by N. tenuis on tomato plants. Nesidiocoris tenuis preferred sesame over tomato plants (except when food was provided only on the tomato plant) and the upper part of the plants, whereas M. pygmaeus preferred tomato to sesame plants (except when food was provided only on the sesame plant) and had no preference for a plant part. Combination of predators N. tenuis and M. pygmaeus allows for better coverage of cultivated plants in terms of occupation of different plant parts and better regulation of T. absoluta populations. Sesamum indicum is a potential companion plant that can be used to significantly reduce N. tenuis damage to tomatoes.

Do assortative mating and immigrant inviability help maintain population genetic structuring of an herbivore on a crop and a wild relative?

Population genetic structuring is common among herbivorous insects and frequently is associated with divergent host plants, such as crops and their wild relatives. Previous studies showed population genetic structuring in corn leafhopper Dalbulus maidis in Mexico, such that the species consists of two sympatric, host plant-associated populations: an abundant and widespread "pestiferous" population on maize (Zea mays mays), and a small and localized "wild" population on perennial teosinte (Zea diploperennis), a maize wild relative with a limited distribution. This study addressed whether assortative mating and immigrant inviability mediate genetic structuring of corn leafhopper by comparing the mating and reproductive successes of pestiferous and wild females that colonize their nonassociated host plants against the successes of females colonizing their associated host plants. Assortative mating was assessed by comparing mating frequencies and premating and mating times among females of each population on each host plant; immigrant inviability was assessed by comparing, across two generations, the fecundity, survival, development time, sex ratio, and population growth rate among leafhopper populations and host plants. Our results showed that on maize, and compared to resident, pestiferous females, wild females were more likely to mate, and greater proportions of their offspring survived to adult stage and were daughters; consequently, the per-generation population growth rate on maize was greater for immigrant, wild leafhoppers compared to resident, pestiferous leafhoppers. Our results suggested that wild leafhoppers emigrating to maize have a fitness advantage over resident, pestiferous leafhoppers, while immigrant pestiferous and resident wild leafhoppers on teosinte have similar fitnesses.

Mixed release of two parasitoids and a polyphagous ladybird as a potential strategy to control the tobacco whitefly Bemisia tabaci.

A mixed species release of parasitoids is used to suppress outbreaks of tobacco whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae); however, this biocontrol may be inhibited by interspecific interactions. We investigated the effects of mixed releases of natural enemies of B. tabaci on predation rates, parasite performance and adult parasitoid emergence under greenhouse conditions. We tested the polyphagous predatory ladybird Harmonia axyridis (Coleoptera: Coccinellidae) and two whitefly-specific parasitoids, namely Encarsia formosa and Encarsia sophia (both, Hymenoptera: Aphelinidae). Harmonia axyridis exhibited the lowest rates of predation when released with each parasitoid than with both parasitoid species together and showed a significant preference for non-parasitized nymphs as prey. Both E. formosa and E. sophia parasitized more B. tabaci when released with the ladybird than when the wasps were released either alone or mixed with the other parasitoid. We also found that the presence of H. axyridis significantly reduced adult parasitoid emergence; the highest rate of adult emergence was obtained with parasitoids released alone. Our results indicate that different combinations of natural enemies can influence observed rates of predation, parasitism, and parasitoid emergence. Therefore, the combination of natural enemies to be used for a particular biological control program should depend on the specific objectives.

Intraguild predation of Geocoris punctipes on Eretmocerus eremicus and its influence on the control of the whitefly Trialeurodes vaporariorum.

BACKGROUND: Geocoris punctipes (Hemiptera: Lygaeidae) and Eretmocerus eremicus (Hymenoptera: Aphelinidae) are whitefly natural enemies. Previously, under laboratory conditions, we showed that G. punctipes engages in intraguild predation (IGP), the attack of one natural enemy by another, on E. eremicus. However, it is unknown whether this IGP interaction takes place under more complex scenarios, such as semi-field conditions. Even more importantly, the effect of this interaction on the density of the prey population requires investigation. Therefore, the present study aimed to establish whether this IGP takes place under semi-field conditions and to determine whether the predation rate of G. punctipes on the whitefly decreases when IGP takes place. RESULTS: Molecular analysis showed that, under semi-field conditions, G. punctipes performed IGP on E. eremicus. However, although IGP did take place, the predation rate by G. punctipes on the whitefly was nevertheless higher when both natural enemies were present together than when the predator was present alone. CONCLUSION: While IGP of G. punctipes on E. eremicus does occur under semi-field conditions, it does not adversely affect whitefly control. The concomitant use of these two natural enemies seems a valid option for inundative biological control programmes of T. vaporariorum in tomato. © 2015 Society of Chemical Industry.

Foraging behaviour of the parasitoid Eretmocerus eremicus under intraguild predation risk by Macrolophus pygmaeus.

BACKGROUND: Intraguild predation (IGP), predation between species that use a common resource, can affect the populations of a pest, of the pest's natural enemy (IG prey) and of the predator of the pest's natural enemy (IG predator). In this study, we determined whether the parasitoid Eretmocerus eremicus (Hymenoptera: Aphelinidae) (IG prey), modifies its foraging behaviour under the risk of IGP by Macrolophus pygmaeus (Hemiptera: Miridae) (IG predator). Parasitoid behaviour was analysed using two bioassays (choice and no-choice) with the following treatments: (i) control, tomato leaf infested with whitefly nymphs; and (ii) PEP, tomato leaf infested with whitefly nymphs and previously exposed to the IG predator; and (iii) PP, tomato leaf infested with whitefly nymphs, with both, the IG predator and the IG prey present. RESULTS: In both bioassays, we found that E. eremicus did not significantly modify the number of ovipositions, time of residence, duration of oviposition or behavioural sequence. However, in the no-choice bioassay, the number of attacks was higher and their duration shorter in the PEP treatment than in the control. CONCLUSION: Our results indicate that the parasitoid may detect IGP risk to a certain extent, but it did not significantly modify its foraging behaviour, suggesting that simultaneous release of the two natural enemies can be successfully employed.

Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites.

Imidacloprid, one of the most commonly used insecticides, is highly toxic to bees and other beneficial insects. The regulatory challenge to determine safe levels of residual pesticides can benefit from information about the time-dependent toxicity of this chemical. Using published toxicity data for imidacloprid for several insect species, we construct time-to-lethal-effect toxicity plots and fit temporal power-law scaling curves to the data. The level of toxic exposure that results in 50% mortality after time t is found to scale as t(1.7) for ants, from t(1.6) to t(5) for honeybees, and from t(1.46) to t(2.9) for termites. We present a simple toxicological model that can explain t(2) scaling. Extrapolating the toxicity scaling for honeybees to the lifespan of winter bees suggests that imidacloprid in honey at 0.25 µg/kg would be lethal to a large proportion of bees nearing the end of their life.

Intraguild predation on the whitefly parasitoid Eretmocerus eremicus by the generalist predator Geocoris punctipes: a behavioral approach.

Intraguild predation (IGP) takes place when natural enemies that use similar resources attack each other. The impact of IGP on biological control can be significant if the survival of natural enemy species is disrupted. In the present study, we assessed whether Geocoris punctipes (Hemiptera: Lygaeidae) engages in IGP on Eretmocerus eremicus (Hymenoptera: Aphelinidae) while developing on whitefly nymphs of Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). In choice and non-choice tests, we exposed G. punctipes to parasitized and non-parasitized whitefly nymphs. We found that G. punctipes does practice IGP on E. eremicus. However, choice tests assessing G. punctipes consumption revealed a significant preference for non-parasitized T. vaporariorum nymphs. Subsequently, we investigated whether E. eremicus females modify their foraging behavior when exposed to conditions involving IGP risk. To assess this, we analyzed wasp foraging behavior under the following treatments: i) whitefly nymphs only (control = C), ii) whitefly nymphs previously exposed to a predator ( = PEP) and, iii) whitefly nymphs and presence of a predator ( = PP). In non-choice tests we found that E. eremicus did not significantly modify its number of attacks, attack duration, oviposition duration, or behavior sequences. However, E. eremicus oviposited significantly more eggs in the PEP treatment. In the PP treatment, G. punctipes also preyed upon adult E. eremicus wasps, significantly reducing their number of ovipositions and residence time. When the wasps were studied under choice tests, in which they were exposed simultaneously to all three treatments, the number of attacks and frequency of selection were similar under all treatments. These results indicate that under IGP risk, E. eremicus maintains several behavioral traits, but can also increase its number of ovipositions in the presence of IG-predator cues. We discuss these findings in the context of population dynamics and biological control.

Cross-kingdom effects of plant-plant signaling via volatile organic compounds emitted by tomato (Solanum lycopersicum) plants infested by the greenhouse whitefly (Trialeurodes vaporariorum).

Volatile organic compounds (VOCs) emitted from plants in response to insect infestation can function as signals for the attraction of predatory/parasitic insects and/or repulsion of herbivores. VOCs also may play a role in intra- and inter-plant communication. In this work, the kinetics and composition of VOC emissions produced by tomato (Solanum lycopersicum) plants infested with the greenhouse whitefly Trialeurodes vaporariorum was determined within a 14 days period. The VOC emission profiles varied concomitantly with the duration of whitefly infestation. A total of 36 different VOCs were detected during the experiment, 26 of which could be identified: 23 terpenoids, plus decanal, decane, and methyl salicylate (MeSA). Many VOCs were emitted exclusively by infested plants, including MeSA and 10 terpenoids. In general, individual VOC emissions increased as the infestation progressed, particularly at 7 days post-infestation (dpi). Additional tunnel experiments showed that a 3 days exposure to VOC emissions from whitefly-infested plants significantly reduced infection by a biotrophic bacterial pathogen. Infection of VOC-exposed plants induced the expression of a likely tomato homolog of a methyl salicylate esterase gene, which preceded the expression of pathogenesis-related protein genes. This expression pattern correlated with reduced susceptibility in VOC-exposed plants. The observed cross-kingdom effect of plant-plant signaling via VOCs probably represents a generalized defensive response that contributes to increased plant fitness, considering that resistance responses to whiteflies and biotrophic bacterial pathogens in tomato share many common elements.

Attraction of the parasitoid Cotesia marginiventris to host (Spodoptera frugiperda) frass is affected by transgenic maize.

We assessed in the laboratory the attraction of the parasitoid Cotesia marginiventris (Cresson) toward odors emitted by conventional maize (Zea mays L. ssp. mays) and Bt (Bacillus thuringiensis) maize seedlings following actual or simulated injury by Spodoptera frugiperda (Smith), the parasitoid's host, and emitted by the host's frass, produced following consumption of conventional or Bt maize seedlings. Females of C. marginiventris exhibited similarly strong responses to conventional and Bt maize seedlings injured by the host or with simulated injury, and these were stronger than responses to clean air. In contrast, the responses of C. marginiventris females were consistently weaker toward host frass derived from Bt maize tissue compared to frass derived from conventional maize tissue. We hypothesized that the weakened response was due to a detrimental effect of Bt endotoxins, present in the Bt maize tissue, on the bacterial community present in the host's gut and frass, including bacteria that produce odors attractive to C. marginiventris. As an initial test of our hypothesis, we compared between the responses of C. marginiventris females to host frass produced following consumption of Bt maize and frass produced from conventional maize which had been treated with an antibiotic (tetracycline) to eliminate host gut bacteria. Our results showed that C. marginiventris females responded similarly weakly to host frass derived from conventional maize tissue treated with antibiotic and to frass derived from Bt maize tissue, treated or untreated with antibiotic, while they responded strongly to frass derived from conventional maize untreated with antibiotic, so provided initial, partial support for our hypothesis. We discussed the weakened response of C. marginiventris females to host frass derived from Bt maize in the context of plausible impacts of transgenic crop cultivars on parasitoid foraging and populations, and the implications for biological control of non-target, polyphagous pests, such as S. frugiperda.

Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment.

Neurotoxic pyrethroid insecticides are widely used for crop protection, and lethal and sublethal perturbations can be expected in beneficial insects. Under laboratory conditions, the lethal and sublethal effects of deltamethrin on the aphid parasitoid Diaeretiella rapae M'Intosh (Hymenoptera: Braconidae) were studied at the mummy stage and in emerging adults. Following a multistep bioassay, analyses were aimed at evaluating the effects of deltamethrin at various crucial steps in the recolonization process following a deltamethrin treatment: Parasitoid pupal development (emergence from the mummies), adult survival, and host-searching capacity. A four-armed olfactometer was used to investigate the effect of deltamethrin on host-searching behavior (a range of concentrations causing 0.4-79.4% mortality was tested), and a Potter tower was used to test the deltamethrin effect with a realistic application method (four concentrations were tested: 0.5, 5.0, 6.25, and 50 g active ingredient [a.i.]/ha). Deltamethrin reduced the percentage of emergence from mummies, but only when exposed to the 50 g a.i./ha concentration. However, for all concentrations tested, the insecticide induced a decrease in longevity after emergence from sprayed mummies and significant adult mortality when parasitoids walked on fresh residues on leaves. Indices were defined and predicted a high mortality and, thus, reduction of recolonization capacities. However, deltamethrin had no effect on orientation behavior toward aphid-infested plants for adults that survived a residual exposure to the insecticide. The impact of deltamethrin on recolonization via pupal emergence and interest in the methodology used are discussed.