Exotic predators can sequester and use novel toxins from exotic non-coevolved prey.

Defensive chemicals of prey can be sequestered by some coevolved predators, which take advantage of prey toxins for their own defence. The increase in the number of invasive species in the Anthropocene has resulted in new interactions among non-coevolved predator and prey species. While novelty in chemical defence may provide a benefit for invasive prey against non-coevolved predators, resident predators with the right evolutionary pre-adaptations might benefit from sequestering these novel defences. Here, we chose a well-known system of invasive species to test whether non-coevolved predators can sequester and use toxins from exotic prey. Together with the invasive prickly pear plants, cochineal bugs (Dactylopius spp.) are spreading worldwide from their native range in the Americas. These insects produce carminic acid, a defensive anthraquinone that some specialized predators sequester for their own defence. Using this system, we first determined whether coccinellids that prey on cochineal bugs in the Mediterranean region tolerated, sequestered, and released carminic acid in reflex bleeding. Then, we quantified the deterrent effect of carminic acid against antagonistic ants. Our results demonstrate that the Australian coccinellid Cryptolaemus montrouzieri sequestered carminic acid, a substance absent in its coevolved prey, from exotic cochineal bugs. When attacked, the predator released this substance through reflex bleeding at concentrations that were deterrent against antagonistic ants. These findings reveal that non-coevolved predators can sequester and use novel toxins from exotic prey and highlights the surprising outcomes of novel interactions that arise from species invasions.

An insect's energy bar: the potential role of plant guttation on biological control.

Plant guttation is an exudation fluid composed of xylem and phloem sap secreted at the margins of leaves of many agricultural crops. Although plant guttation is a widespread phenomenon, its effect on natural enemies remains largely unexplored. A recent study showed that plant guttation can be a reliable nutrient-rich food source for natural enemies, affecting their communities in highbush blueberries. This review highlights the potential role of plant guttation as a food source for natural enemies, with a particular emphasis on its nutritional value, effects on insect communities, and potential use in conservation biological control. We also discuss possible negative implications and conclude with some open questions and future directions for research.

Honeydew management to promote biological control.

Honeydew is the excretion of plant-feeding hemipterans and it is one of the most abundant source of carbohydrates for parasitoids and predators in agroecosystems. Being so abundant, honeydew mediates direct and indirect interactions that affect biological control. We describe these interactions and identify honeydew-management strategies to reduce pest pressure. First, the presence of nondamaging honeydew producers in cover crops and hedges increases the efficacy of parasitoids and predators. Second, breaking the mutualism between ants and honeydew-producing pests with alternative sugar sources promotes biological control of these pests. Third, we propose to explore honeydew volatiles to attract biological control agents and repel pests, as well as to induce plant defenses. Finally, we urge reducing the use of systemic pesticides that contaminate honeydew and negatively affect biological control agents that feed on it. Overall, we propose that honeydew management is integrated in pest management programs to contribute to sustainable agriculture.

Exclusion of Mediterranean ant species enhances biological control of the invasive mealybug Delottococcus aberiae in citrus.

BACKGROUND: Delottococcus aberiae is an invasive mealybug that produces severe damage in Spanish citrus. This mealybug has established a mutualistic relationship with native Mediterranean ant species that may limit biological control of this pest. Herein, we evaluated the effect of tending ants on the biological control of D. aberiae. To do this, we compared: (i) the density of D. aberiae, (ii) the density of its natural enemies, and (iii) the damage produced by the mealybug in trees with (control) and without ants (ants excluded with sticky barriers) in two citrus orchards across two consecutive years. RESULTS: Lasius grandis was the most abundant ant species in both orchards and represented more than 95% of the ants tending D. aberiae in control trees. Spiders and lacewings were the most abundant predators observed in mealybug colonies, and the exclusion of mutualistic ants increased their abundance. Moreover, in control trees, ant activity throughout the year was negatively correlated with the relative abundance of predators (number of predators per mealybug). No parasitoids were recovered during field experiments. Ant exclusion reduced the density of D. aberiae and the ratio of damaged fruit at harvest across years and orchards. CONCLUSIONS: This work corroborates the previous finding that D. aberiae benefits from its mutualistic relationship with L. grandis, probably because the presence of ants reduced the abundance of generalist predators. This mutualism can be disrupted using physical barriers on on the trunk. Further research should assess other methods of ant control that are more economic and feasible for citrus producers. © 2023 Society of Chemical Industry.

Competitive interactions in insect parasitoids: effects of microbial symbionts across tritrophic levels.

Competition for hosts is a common ecological interaction in insect parasitoids. In the recent years, it has become increasingly evident that microorganisms can act as 'hidden players' in parasitoid ecology. In this review, we propose that parasitoid competition should take into consideration the microbial influence. In particular, we take a tritrophic perspective and discuss how parasitoid competition can be modulated by microorganisms associated with the parasitoids, their herbivore hosts, or the plants attacked by the herbivores. Although research is still in its infancy, recent studies have shown that microbial symbionts can modulate the contest outcome. The emerging pattern is that microorganisms not only affect the competitive traits of parasitoids but also the fighting arena (i.e. the herbivore host and its food plant), in which competition takes place. We have also identified important gaps in the literature that should be addressed in future studies to advance our understanding about parasitoid competition.

The effects of ants on pest control: a meta-analysis.

Environmental impacts of conventional agriculture have generated interest in sustainable agriculture. Biological pest control is a fundamental tool, and ants are key players providing ecological services, as well as some disservices. We have used a meta-analytical approach to investigate the contribution of ants to biological control, considering their effects on pest and natural enemy abundance, plant damage and crop yield. We also evaluated whether the effects of ants are modulated by traits of ants, pests and other natural enemies, as well as by field size, crop system and experiment duration. Overall (considering all meta-analyses), from 52 studies on 17 different crops, we found that ants decrease the abundance of non-honeydew-producing pests, decrease plant damage and increase crop yield (services). In addition, ants decrease the abundance of natural enemies, mainly the generalist ones, and increase honeydew-producing pest abundance (disservices). We show that the pest control and plant protection provided by ants are boosted in shaded crops compared to monocultures. Furthermore, ants increase crop yield in shaded crops, and this effect increases with time. Finally, we bring new insights such as the importance of shaded crops to ant services, providing a good tool for farmers and stakeholders considering sustainable farming practices.

Insecticide-contaminated honeydew: risks for beneficial insects.

Honeydew is the sugar-rich excretion of phloem-feeding hemipteran insects such as aphids, mealybugs, whiteflies, and psyllids, and can be a main carbohydrate source for beneficial insects in some ecosystems. Recent research has revealed that water-soluble, systemic insecticides contaminate honeydew excreted by hemipterans that feed on plants treated with these insecticides. This contaminated honeydew can be toxic to beneficial insects, such as pollinators, parasitic wasps and generalist predators that feed on it. This route of exposure has now been demonstrated in three plant species, for five systemic insecticides and four hemipteran species; therefore, we expect this route to be widely available in some ecosystems. In this perspective paper, we highlight the importance of this route of exposure by exploring: (i) potential pathways through which honeydew might be contaminated with insecticides; (ii) hemipteran families that are more likely to excrete contaminated honeydew; and (iii) systemic insecticides with different modes of action that might contaminate honeydew through the plant. Furthermore, we analyse several model scenarios in Europe and/or the USA where contaminated honeydew could be problematic for beneficial organisms that feed on this ubiquitous carbohydrate source. Finally, we explain why this route of exposure might be important when exotic, invasive, honeydew-producing species are treated with systemic insecticides. Overall, this review opens a new area of research in the field of ecotoxicology to understand how insecticides can reach non-target beneficial insects. In addition, we aim to shed light on potential undescribed causes of insect declines in ecosystems where honeydew is an important carbohydrate source for insects, and advocate for this route of exposure to be included in future environmental risk assessments.

Insights into the origin of the invasive populations of Trioza erytreae in Europe using microsatellite markers and mtDNA barcoding approaches.

The African citrus psyllid Trioza erytreae is one of the major threats to citrus industry as the vector of the incurable disease known as huanglongbing (HLB) or citrus greening. The psyllid invaded the northwest of the Iberian Peninsula 6 years ago. The invasion alarmed citrus growers in the Mediterranean basin, the largest citrus producing area in Europe, which is still free of HLB. Before our study, no research had been carried out on the genetic diversity of T. erytreae populations that have invaded the Iberian Peninsula and the archipelagos of the Macaronesia (Madeira and the Canary Islands). In this study, combining microsatellites markers and mtDNA barcoding analysis, we characterize the genetic diversity, structure and maternal relationship of these new invasive populations of T. erytreae and those from Africa. Our results suggest that the outbreaks of T. erytreae in the Iberian Peninsula may have derived from the Canary Islands. The populations of T. erytreae that invaded Macaronesia and the Iberian Peninsula are likely to have originated from southern Africa. We anticipate our results to be a starting point for tracking the spread of this invasive pest outside of Africa and to be important for optimizing contingency and eradication plans in newly invaded and free areas.

Commodity risk assessment of Citrus L. fruits from South Africa for Thaumatotibia leucotreta under a systems approach.

The European Commission requested to the EFSA Panel on Plant Health to evaluate a dossier from South Africa where the application of the systems approach to mitigate the risk of entry of the false codling moth, Thaumatotibia leucotreta (Lepidoptera: Tortricidae), into the EU when trading citrus fruits is explained. After collecting additional evidence from the Department of Agriculture, Land Reform and Rural Development of South Africa, and reviewing the published literature, the Panel performed an assessment on the likelihood of pest freedom for T. leucotreta on citrus fruits at the point of entry in the EU considering the proposed systems approach. An expert judgement is given on the likelihood of pest freedom following the evaluation of the risk mitigation measures on T. leucotreta, including any uncertainties. There are three options (i.e. A, B and C) within the systems approach followed in South Africa that differentiate mainly in the sampling intensity in the field and the packing house as well as in temperature conditions during shipment. Therefore, three independent elicitations were conducted, one for each option. The main uncertainties were: (1) whether sampling once per orchard is representative for subsequent harvests (within 4 weeks) from the same orchard; (2) the correct implementation of the temperature regimes during shipment; (3) the mortality rate in fruit estimated for the different temperature regimes. The Expert Knowledge Elicitation indicated with 95% certainty that 9,182 out of 10,000 pallets for option A, 8,478 out of 10,000 pallets for option B, and 9,743 out of 10,000 pallets for option C will be free from T. leucotreta. In light of the additional information provided by South Africa once the elicitations were performed, it became apparent that the setting temperature during shipment was not achieved in 12 out of 14 cases of interceptions. Therefore, there is increased uncertainty on pest freedom. The Panel identified the weaknesses associated with the risk mitigation measures in the systems approach and made recommendations that could increase its effectiveness.

Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents.

Seed coating ('seed treatment') is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.

Sex, males, and hermaphrodites in the scale insect Icerya purchasi.

Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here, we investigate the cottony cushion scale, Icerya purchasi, one of only three reported cases of androdioecy in insects. In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, males are ocassionally observed as well. In a large genetic analysis, we show for the first time that, although self-fertilization appears to be the primary mode of reproduction, rare outbreeding events do occur in natural populations, supporting the hypothesis that hermaphrodites mate with males and hence androdioecy is the mating system of I. purchasi. Thus, this globally invasive pest insect appears to enjoy the colonization advantages of a selfing organism while also benefitting from periodic reintroduction of genetic variation through outbreeding with males.

Commodity risk assessment of Citrus L. fruits from Israel for Thaumatotibia leucotreta under a systems approach.

The European Commission requested EFSA Panel on Plant Health to evaluate a dossier from Israel in which the application of the systems approach to mitigate the risk of entry of Thaumatotibia leucotreta to the EU when trading citrus fruits is described. After collecting additional evidence from the Plant Protection and Inspection Services (PPIS) of Israel, and reviewing the published literature, the Panel performed an assessment on the likelihood of pest freedom for T. leucotreta on citrus fruits at the point of entry in the EU considering the Israelian systems approach. An expert judgement is given on the likelihood of pest freedom following the evaluation of the risk mitigation measures on T. leucotreta, including any uncertainties. The Expert Knowledge Elicitation indicated, with 95% certainty that between 9,863 and 10,000 citrus fruits per 10,000 will be free from this pest. The Panel also evaluated each risk mitigation measure in the systems approach and identified any weaknesses associated with them. Specific actions are identified that could increase the efficacy of the systems approach.

Parasitic wasps avoid ant-protected hemipteran hosts via the detection of ant cuticular hydrocarbons.

One of the most studied and best-known mutualistic relationships between insects is that between ants and phloem-feeding insects. Ants feed on honeydew excreted by phloem-feeding insects and, in exchange, attack the phloem feeders' natural enemies, including parasitic wasps. However, parasitic wasps are under selection to exploit information on hazards and avoid them. Here, we tested whether parasitic wasps detect the previous presence of ants attending colonies of phloem feeders. Behavioural assays demonstrate that wasps left colonies previously attended by ants more frequently than control colonies. This behaviour has a potential cost for the parasitic wasp as females inserted their ovipositor in fewer hosts per colony. In a further bioassay, wasps spent less time on papers impregnated with extracts of the ant cues than on control papers. Gas chromatography coupled with mass spectrometry analyses demonstrated that ants left a blend of cuticular hydrocarbons when they attended colonies of phloem feeders. These cuticular hydrocarbons are deposited passively when ants search for food. Overall, these results suggest, for the first time, that parasitic wasps of honeydew producers detect the previous presence of mutualistic ants through contact infochemicals. We anticipate such interactions to be widespread and to have implications in numerous ecosystems, as phloem feeders are usually tended by ants.

IPM-recommended insecticides harm beneficial insects through contaminated honeydew.

The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrusvladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew.

Plant guttation provides nutrient-rich food for insects.

Plant guttation is a fluid from xylem and phloem sap secreted at the margins of leaves from many plant species. All previous studies have considered guttation as a water source for insects. Here, we hypothesized that plant guttation serves as a reliable and nutrient-rich food source for insects with effects on their communities. Using highbush blueberries as a study system, we demonstrate that guttation droplets contain carbohydrates and proteins. Insects from three feeding lifestyles, a herbivore, a parasitic wasp and a predator, increased their longevity and fecundity when fed on these guttation droplets compared to those fed on control water. Our results also show that guttation droplets, unlike nectar, are present on leaves during the entire growing season and are visited by numerous insects of different orders. In exclusion-field experiments, the presence of guttation modified the insect community by increasing the number of predators and parasitic wasps that visited the plants. Overall, our results demonstrate that plant guttation is highly reliable, compared to other plant-derived food sources such as nectar, and that it increases the communities and fitness of insects. Therefore, guttation represents an important plant trait with profound implications on multi-trophic insect-plant interactions.

Neonicotinoids in excretion product of phloem-feeding insects kill beneficial insects.

Pest control in agriculture is mainly based on the application of insecticides, which may impact nontarget beneficial organisms leading to undesirable ecological effects. Neonicotinoids are among the most widely used insecticides. However, they have important negative side effects, especially for pollinators and other beneficial insects feeding on nectar. Here, we identify a more accessible exposure route: Neonicotinoids reach and kill beneficial insects that feed on the most abundant carbohydrate source for insects in agroecosystems, honeydew. Honeydew is the excretion product of phloem-feeding hemipteran insects such as aphids, mealybugs, whiteflies, and psyllids. We allowed parasitic wasps and pollinating hoverflies to feed on honeydew from hemipterans feeding on trees treated with thiamethoxam or imidacloprid, the most commonly used neonicotinoids. LC-MS/MS analyses demonstrated that both neonicotinoids were present in honeydew. Honeydew with thiamethoxam was highly toxic to both species of beneficial insects, and honeydew with imidacloprid was moderately toxic to hoverflies. Collectively, our data provide strong evidence for honeydew as a route of insecticide exposure that may cause acute or chronic deleterious effects on nontarget organisms. This route should be considered in future environmental risk assessments of neonicotinoid applications.

Nonreproductive Effects of Insect Parasitoids on Their Hosts.

The main modes of action of insect parasitoids are considered to be killing their hosts with egg laying followed by offspring development (reproductive mortality), and adults feeding on hosts directly (host feeding). However, parasitoids can also negatively affect their hosts in ways that do not contribute to current or future parasitoid reproduction (nonreproductive effects). Outcomes of nonreproductive effects for hosts can include death, altered behavior, altered reproduction, and altered development. On the basis of these outcomes and the variety of associated mechanisms, we categorize nonreproductive effects into ( a) nonconsumptive effects, ( b) mutilation, ( c) pseudoparasitism, ( d) immune defense costs, and ( e) aborted parasitism. These effects are widespread and can cause greater impacts on host populations than successful parasitism or host feeding. Nonreproductive effects constitute a hidden dimension of host-parasitoid trophic networks, with theoretical implications for community ecology as well as applied importance for the evaluation of ecosystem services provided by parasitoid biological control agents.

Seasonal Distribution and Movement of the Invasive Pest Delottococcus aberiae (Hemiptera: Pseudococcidae) Within Citrus Tree: Implications for Its Integrated Management.

Delottococcus aberiae (De Lotto) (Hemiptera: Pseudococcidae) is the most recent species of mealybug introduced to Spain that is affecting citrus. The feeding behavior of D. aberiae causes severe direct damage to citrus fruits, distorting their shape and/or causing reduction in size. There is no information available regarding its distribution within the citrus trees. The main objective of this study was to describe the seasonal distribution of D. aberiae within citrus trees and its migration patterns on the plants. Ten citrus orchards from eastern Spain were periodically sampled during 3 yr. In each orchard, the mealybug was sampled in different infested strata (canopy, trunk, and soil) and canopy structures (flower, fruit, leaf, and twig). Results showed that, within the sampled strata, D. aberiae was mostly in the canopy. Within the canopy, the feeding location of D. aberiae changed throughout the year. D. aberiae overwintered in the twigs and moved to the flowers and fruits in spring. Once there, its populations started to increase exponentially until August. From February to September, 5-30% of the mealybugs migrated to the trunk and soil. These results will facilitate an early detection of the pest in the areas where it is spreading and improve sampling protocols and pesticide applications.

Defensive behaviors of the new mealybug citrus pest, Delottococcus aberiae (Hemiptera: Pseudococcidae), against three generalist parasitoids.

Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae) is an invasive mealybug that has become a citrus pest in Europe. This mealybug species causes serious damage because it deforms the fruits. Here, we studied the defensive behavior of D. aberiae when it was attacked by three parasitoid species: Acerophagus angustifrons (Gahan), Anagyrus sp. near pseudoccoci (Girault), and Leptomastix algirica Trjapitzin (Hymenoptera: Encyrtidae). Anagyrus sp. near pseudoccoci and L. algirica detected and accepted nymphs and adult females of D. aberiae, whereas A. angustifrons only accepted adults. We recorded four defensive responses of D. aberiae to parasitoid attacks: abdominal flipping, swiveling around the inserted stylet, withdrawing the stylet and walking away, and, occasionally, they secreted ostiolar fluids. Despite these defensive behaviors, the mealybug did not escape parasitism from any of the tested parasitoids, even though A. angustifrons needed more than 15 min to parasitize. We also analyzed the nutritional value of the honeydew excreted by D. aberiae for A. angustifrons and A. sp. near pseudococci. Females and males of these parasitoids lived more than 28 d when fed sucrose, but they lived fewer than 3 d when fed D. aberiae honeydew. Therefore, D. aberiae excretes honeydew of poor quality for parasitoids. The consequences of these biological traits of D. aberiae for its biological control are discussed.