Cereal Aphid Parasitoids in Europe (Hymenoptera: Braconidae: Aphidiinae): Taxonomy, Biodiversity, and Ecology.

Cereals are very common and widespread crops in Europe. Aphids are a diverse group of herbivorous pests on cereals and one of the most important limiting factors of cereal production. Here, we present an overview of knowledge about the taxonomy, biodiversity, and ecology of cereal aphid parasitoids in Europe, an important group of natural enemies contributing to cereal aphid control. We review the knowledge obtained from the integrative taxonomy of 26 cereal aphid primary parasitoid species, including two allochthonous species (Lysiphlebus testaceipes and Trioxys sunnysidensis) and two recently described species (Lipolexis labialis and Paralipsis brachycaudi). We further review 28 hyperparasitoid species belonging to three hymenopteran superfamilies and four families (Ceraphronoidea: Megaspillidae; Chalcidoidea: Pteromalidae, Encyrtidae; Cynipoidea: Figitidae). We also compile knowledge on the presence of secondary endosymbionts in cereal aphids, as these are expected to influence the community composition and biocontrol efficiency of cereal aphid parasitoids. To study aphid-parasitoid-hyperparasitoid food webs more effectively, we present two kinds of DNA-based approach: (i) diagnostic PCR (mainly multiplex PCR), and (ii) DNA sequence-based methods. Finally, we also review the effects of landscape complexity on the different trophic levels in the food webs of cereal aphids and their associated parasitoids, as well as the impacts of agricultural practices and environmental variation.

The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis.

Floral plantings are promoted to foster ecological intensification of agriculture through provisioning of ecosystem services. However, a comprehensive assessment of the effectiveness of different floral plantings, their characteristics and consequences for crop yield is lacking. Here we quantified the impacts of flower strips and hedgerows on pest control (18 studies) and pollination services (17 studies) in adjacent crops in North America, Europe and New Zealand. Flower strips, but not hedgerows, enhanced pest control services in adjacent fields by 16% on average. However, effects on crop pollination and yield were more variable. Our synthesis identifies several important drivers of variability in effectiveness of plantings: pollination services declined exponentially with distance from plantings, and perennial and older flower strips with higher flowering plant diversity enhanced pollination more effectively. These findings provide promising pathways to optimise floral plantings to more effectively contribute to ecosystem service delivery and ecological intensification of agriculture in the future.

Facultative bacterial endosymbionts shape parasitoid food webs in natural host populations: A correlative analysis.

Facultative bacterial endosymbionts can protect their aphid hosts from natural enemies such as hymenopteran parasitoids. As such, they have the capability to modulate interactions between aphids, parasitoids and hyperparasitoids. However, the magnitude of these effects in natural aphid populations and their associated parasitoid communities is currently unknown. Moreover, environmental factors such as plant fertilization and landscape complexity are known to affect aphid-parasitoid interactions but it remains unclear how such environmental factors affect the interplay between aphids, parasitoids and endosymbionts. Here, we tested whether facultative endosymbionts confer protection to parasitoids in natural populations of the English grain aphid, Sitobion avenae, and if this is affected by plant fertilization and landscape complexity. Furthermore, we examined whether the effects of facultative endosymbionts can cascade up to the hyperparasitoid level and increase primary-hyperparasitoid food web specialization. Living aphids and mummies were collected in fertilized and unfertilized plots within 13 wheat fields in Central Germany. We assessed the occurrence of primary parasitoid, hyperparasitoid and endosymbiont species in aphids and mummies using a newly established molecular approach. Facultative endosymbiont infection rates were high across fields (~80%), independent of whether aphids were parasitized or unparasitized. Aphid mummies exhibited a significantly lower share of facultative endosymbiont infection (~38%). These findings suggest that facultative endosymbionts do not affect parasitoid oviposition behaviour, but decrease parasitoid survival in the host. Facultative endosymbiont infection rates were lower in mummies collected from fertilized compared to unfertilized plants, indicating that plant fertilization boosts the facultative endosymbiont protective effect. Furthermore, we found strong evidence for species-specific and negative cascading effects of facultative endosymbionts on primary and hyperparasitoids, respectively. Facultative endosymbionts impacted parasitoid assemblages and increased the specialization of primary-hyperparasitoid food webs: these effects were independent from and much stronger than other environmental factors. The current findings strongly suggest that facultative endosymbionts act as a driving force in aphid-parasitoid-hyperparasitoid networks: they shape insect community composition at different trophic levels and modulate, directly and indirectly, the interactions between aphids, parasitoids and their environment.

Evaluation of three molecular markers for identification of European primary parasitoids of cereal aphids and their hyperparasitoids.

Aphids are major pests of cereal crops and a suite of hymenopteran primary parasitoids play an important role in regulating their populations. However, hyperparasitoids may disrupt the biocontrol services provided by primary parasitoids. As such, understanding cereal aphid-primary parasitoid-hyperparasitoid interactions is vital for a reliable parasitoid-based control of cereal aphids. For this, the ability to identify the different primary and hyperparasitoid species is necessary. Unfortunately, this is often difficult due to a lack of morphologically diagnostic features. DNA sequence-based species identification of parasitoids can overcome these hurdles. However, comprehensive DNA sequence information is lacking for many of these groups, particularly for hyperparasitoids. Here we evaluate three genes [cytochrome c oxidase subunit I (COI), 16S ribosomal RNA (16S) and 18S ribosomal RNA (18S)] for their suitability to identify 24 species of primary parasitoids and 16 species of hyperparasitoids associated with European cereal aphids. To identify aphelinid primary parasitoid species and hyperparasitoids, we found 16S to be more suitable compared to COI sequences. In contrast, the Aphidiinae are best identified using COI due to better species-level resolution and a more comprehensive DNA sequence database compared to 16S. The 18S gene was better suited for group-specific identification of parasitoids, but did not provide resolution at the species level. Our results provide a DNA sequence database for cereal aphid primary parasitoids and their associated hyperparasitoids in Central Europe, which will allow further improvement of our understanding of cereal aphid-primary parasitoid-hyperparasitoid interactions in relation to aphid biological control.

An effective molecular approach for assessing cereal aphid-parasitoid-endosymbiont networks.

Molecular approaches are increasingly being used to analyse host-parasitoid food webs as they overcome several hurdles inherent to conventional approaches. However, such studies have focused primarily on the detection and identification of aphids and their aphidiid primary parasitoids, largely ignoring primary parasitoid-hyperparasitoid interactions or limiting these to a few common species within a small geographical area. Furthermore, the detection of bacterial secondary endosymbionts has not been considered in such assays despite the fact that endosymbionts may alter aphid-parasitoid interactions, as they can confer protection against parasitoids. Here we present a novel two-step multiplex PCR (MP-PCR) protocol to assess cereal aphid-primary parasitoid-hyperparasitoid-endosymbiont interactions. The first step of the assay allows detection of parasitoid DNA at a general level (24 primary and 16 hyperparasitoid species) as well as the species-specific detection of endosymbionts (3 species) and cereal aphids (3 species). The second step of the MP-PCR assay targets seven primary and six hyperparasitoid species that commonly occur in Central Europe. Additional parasitoid species not covered by the second-step of the assay can be identified via sequencing 16S rRNA amplicons generated in the first step of the assay. The approach presented here provides an efficient, highly sensitive, and cost-effective (~consumable costs of 1.3 € per sample) tool for assessing cereal aphid-parasitoid-endosymbiont interactions.