BUSCADOR RECOLECTA

Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae) is one of the latest invasive mealybugs in Europe. It causes severe fruit distortion and reduced fruit size leading into important economic losses in citrus. Cryptolaemus montrouzieri (Mulsant) (Coleoptera: Coccinellidae) is probably one of the most-used predators of mealybugs in biological control programs worldwide. However, its impact on D. aberiae is still unknown. Here, we conducted a two-year field study in nine citrus orchards located in eastern Spain in order to describe the population dynamics of D. aberiae and C. montrouzieri and evaluate the effect of the predator on D. aberiae using different approaches. Our results showed that C. montrouzieri and D. aberiae had two main synchronised population peaks per year: early spring and summer. Although D. aberiae and C. montrouzieri seasonal trends were synchronised, C. montrouzieri neither reduced mealybug
density within the same year nor prevented fruit damage, which occurs early in the season. Moreover, D. aberiae population growth rates were not correlated with C. montrouzieri density. When two consecutive years were analyzed, the increase of D. aberiae in the second year was negatively correlated with the density of C. montrouzieri in summer of the previous year. Based on our two years of data, C. montrouzieri was not able to regulate D. aberiae on its own or prevent the damages produced by the mealybug but might become a valuable addition to the natural enemy guild when combined with other natural enemies and rational control measures.

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 Anagyrus vladimiri. 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.

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
thatwasps 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 withmass 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.

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.

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.

The invasive mealybug Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae) has become a key pest in Mediterranean citrus. This mealybug species excretes honeydew that can be consumed by ants, which may give rise to mutualistic relationships and increase the invasibility of this exotic pest. Here, we studied the interaction between D. aberiae and ants in 16 citrus orchards located in the main citrus-growing area of Spain (Valencia) during two consecutive years. Four native ant species were observed feeding on D. aberiae honeydew, and Lasius grandis Forel (Hymenoptera: Formicidae) represented more than 95% of these ants. Lasius grandis was observed attending D. aberiae throughout the year and in all the orchard
sites where the mealybug was present. Mealybug colony size had a positive effect on both relative and absolute ant-attendance by L. grandis, but these interactions varied across seasons. Moreover, we found a positive correlation between L. grandis activity and D. aberiae density in all citrus orchards. Our results suggest that the native ant L. grandis and the invasive pest D. aberiae have established a mutualistic association that promotes the establishment and accelerate the invasion of D. aberiae in Spanish citrus orchards. Further research with the aim of evaluating whether the management of this ant species can improve the control of D. aberiae in citrus would be recommended.

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 the trunk. Further research should assess other methods of ant control that are more economic and feasible for citrus producers.

Pseudococcus longispinus representa la principal plaga en el cultivo de caqui en España. Debido a la problemática que conlleva el uso de insecticidas y la baja eficacia que tienen contra esta plaga, es necesario implementar estrategias basadas en el control biológico para reducir su abundancia. Los
parasitoides se consideran agentes de control biológico clave para el control de pseudocóccidos. En
este trabajo se ha estudiado el complejo de parasitoides que ataca a P. longispinus en caquis de la
Comunidad Valenciana. El parasitismo alcanzó su máximo en otoño, cuando la plaga es más abundante.
La mayoría de pseudocóccidos parasitados se encontraban en estados de desarrollo avanzado: ninfas de tercer estadío y hembras adultas. El parasitoide más abundante y ampliamente distribuido fue Anagyrus fusciventris. Sin embargo, el parasitismo fue muy variable entre parcelas y años. Esta eficacia variable puede deberse a varios factores como son los hiperparasitoides, las hormigas y los insecticidas. Actualmente, el IVIA está trabajando para mejorar la eficacia de este parasitoide.

The simplification of agricultural landscapes has been associated with an increase in pest pressure. While monocultures increase the resources available for pests and may facilitate their dispersion, the lack of non-crop habitats may reduce the resources available for pest natural enemies. Herein, we tested which of these hypotheses, namely ‘resource concentration’ and ‘natural enemies’, can better explain the abundance of invasive mealybug pests in two subtropical fruit crops. For this aim, 17 persimmon orchards and 16 citrus orchards were sampled during three different seasons across two consecutive years. Using a model selection approach, we assessed the effects of the surrounding landscape (proportion of focal crops and semi-natural habitats at different distances) and inter-row ground cover vegetation on the abundance of mealybugs and their natural enemies. The proportion of focal crop in the landscape increased the abundance of mealybugs attacking both crops. This effect was found at closer distances (up to ~600 m) in citrus and at both closer and further distances (up to 1250 m) in persimmon. Non-crop habitats, both surrounding semi-natural habitats and ground cover vegetation, decreased the abundance of mealybugs by increasing the activity of their parasitoids in persimmon. Conversely, non-crop habitats did not decrease the abundance of the main mealybug species attacking citrus, likely because this mealybug species was not attacked by native or naturalized parasitoids. Synthesis and applications: Our models show that the increase in habitat heterogeneity at local and landscape scales can reduce the abundance of invasive mealybugs in subtropical crops via ‘resource concentration’ and ‘natural enemies’ mechanisms. Therefore, habitat diversification strategies should be considered in the conservation biological control of invasive mealybugs. Importantly, our findings also show that the presence of efficient natural enemies is critical to maximize their control through habitat diversification strategies.

The long-tailed mealybug, Pseudococcus longispinus, represents a threat for several crops worldwide and has become the main pest of Mediterranean persimmon. Parasitoids are the primary natural enemies of P. longispinus, but their efficacy is highly variable among crops and countries. Here, we tested whether hyperparasitoids hinder the biological control of P. longispinus in Mediterranean persimmon. For this aim, we sampled 16 orchards across two consecutive years and measured the impact of primary parasitoids and hyperparasitoids on P. longispinus. Anagyrus fusciventris was the most abundant and widely distributed primary parasitoid. Population growth rate of the mealybug became negative when parasitism was higher than 30%. The hyperparasitoids Chartocerus sp. and Prochiloneurus sp. emerged mostly from large mealybug mummies that were used by A. fusciventris females. However, and contrary to our hypothesis, hyperparasitism did not affect the population growth rate of P. longispinus within the same year, suggesting that the high abundance of hyperparasitoids did not disrupt the biological control of this invasive mealybug. Based on these results, we propose several strategies based on conservation and augmentative biological control to improve the management of P. longispinus in persimmon.