Anne Le Ralec

The conflicting relationships between aphids and men: A review of aphid damage and control strategies

In this review, after giving some figures on the economic impact of aphids on agricultural production, we describe the different mechanisms leading to yield losses (direct damage due to sieve drain and plant reaction, indirect damage, often the most important, due to virus transmission). Then, after a history of chemical control and of its limits, the main control strategies (chemical control with decision rules, plant resistance, biological control, farming practices) are reviewed in the light of an integrated pest management approach. Several topics tackled in this article are exemplified for cereal aphids, which are among the most important in Europe as direct feeders and virus vectors.

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 April 2010-31 May 2010

This article documents the addition of 396 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Anthocidaris crassispina, Aphis glycines, Argyrosomus regius, Astrocaryum sciophilum, Dasypus novemcinctus, Delomys sublineatus, Dermatemys mawii, Fundulus heteroclitus, Homalaspis plana, Jumellea rossii, Khaya senegalensis, Mugil cephalus, Neoceratitis cyanescens, Phalacrocorax aristotelis, Phytophthora infestans, Piper cordulatum, Pterocarpus indicus, Rana dalmatina, Rosa pulverulenta, Saxifraga oppositifolia, Scomber colias, Semecarpus kathalekanensis, Stichopus monotuberculatus, Striga hermonthica, Tarentola boettgeri and Thermophis baileyi. These loci were cross‐tested on the following species: Aphis gossypii, Sooretamys angouya, Euryoryzomys russatus, Fundulus notatus, Fundulus olivaceus, Fundulus catenatus, Fundulus majalis, Jumellea fragrans, Jumellea triquetra Jumellea recta, Jumellea stenophylla, Liza richardsonii, Piper marginatum, Piper aequale, Piper darienensis, Piper dilatatum, Rana temporaria, Rana iberica, Rana pyrenaica, Semecarpus anacardium, Semecarpus auriculata, Semecarpus travancorica, Spondias acuminata, Holigarna grahamii, Holigarna beddomii, Mangifera indica, Anacardium occidentale, Tarentola delalandii, Tarentola caboverdianus and Thermophis zhaoermii.

Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae)

Reliable identification of Aphidiinae species (Braconidae) is a prerequisite for conducting studies on aphid–parasitoid interactions at the community level. However, morphological identification of Aphidiinae species remains problematic even for specialists and is almost impossible with larval stages. Here, we compared the efficiency of two molecular markers [mitochondrial cytochrome c oxydase I (COI) and nuclear long wavelength rhodopsin (LWRh)] that could be used to accurately identify about 50 species of Aphidiinae that commonly occur in aphid–parasitoid networks in northwestern Europe. We first identified species on a morphological basis and then assessed the consistency of genetic and morphological data. Probably because of mitochondrial introgression, Aphidius ervi and A. microlophii were indistinguishable on the basis of their COI sequences, whereas LWRh sequences discriminated these species. Conversely, because of its lower variability, LWRh failed to discriminate two pairs of species (Aphidius aquilus, Aphidius salicis, Lysiphlebus confusus and Lysiphlebus fabarum). Our study showed that no unique locus but a combination of two genes should be used to accurately identify members of Aphidiinae.

Evolutionary ecology of the interactions between aphids and their parasitoids

Many organisms, including entomopathogenous fungi, predators or parasites, use aphids as ressources. Parasites of aphids are mostly endoparasitoid insects, i.e. insects which lay eggs inside the body of an other insect which will die as a result of their development. In this article, we review the consequences of the numerous pecularities of aphid biology and ecology for their endoparasitoids, notably the Aphidiinae (Hymenoptera: Braconidae). We first examine the various mechanisms used by aphids for defence against these enemies. We then explore the strategies used by aphidiine parasitoids to exploit their aphid hosts. Finally, we consider the responses of both aphids and parasitoids to ecological constraints induced by seasonal cycles and to environmental variations linked to host plants and climate. The fundamental and applied interest of studying these organisms is discussed.

Molecular analysis reveals high compartmentalization in aphid-primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats.

The ecosystem service of insect pest regulation by natural enemies, such as primary parasitoids, may be enhanced by the presence of uncultivated, semi‐natural habitats within agro‐ecosystems, although quantifying such host–parasitoid interactions is difficult. Here, we use rRNA 16S gene sequencing to assess both the level of parasitism by Aphidiinae primary parasitoids and parasitoid identity on a large sample of aphids collected in cultivated and uncultivated agricultural habitats in Western France. We used these data to construct ecological networks to assess the level of compartmentalization between aphid and parasitoid food webs of cultivated and uncultivated habitats. We evaluated the extent to which uncultivated margins provided a resource for parasitoids shared between pest and nonpest aphids. We compared the observed quantitative ecological network described by our molecular approach to an empirical qualitative network based on aphid–parasitoid interactions from traditional rearing data found in the literature. We found that the molecular network was highly compartmentalized and that parasitoid sharing is relatively rare between aphids, especially between crop and noncrop compartments. Moreover, the few cases of putative shared generalist parasitoids were questionable and could be due to the lack of discrimination of cryptic species or from intraspecific host specialization. Our results suggest that apparent competition mediated by Aphidiinae parasitoids is probably rare in agricultural areas and that the contribution of field margins as a source of these biocontrol agents is much more limited than expected. Further large‐scale (spatial and temporal) studies on other crops and noncrop habitats are needed to confirm this.

A universal method for the detection and identification of Aphidiinae parasitoids within their aphid hosts.

Molecular methods are increasingly used to detect and identify parasites in their hosts. However, existing methods are generally not appropriate for studying complex host–parasite interactions because they require prior knowledge of species composition. DNA barcoding is a molecular method that allows identifying species using DNA sequences as an identification key. We used DNA amplification with primers common to aphid parasitoids and sequencing of the amplified fragment to detect and identify parasitoids in their hosts, without prior knowledge on the species potentially present. To implement this approach, we developed a method based on 16S rRNA mitochondrial gene and LWRh nuclear gene. First, we designed two primer pairs specific to Aphidiinae (Hymenoptera), the main group of aphid parasitoids. Second, we tested whether the amplified regions could correctly identify Aphidiinae species and found that 61 species were accurately identified of 75 tested. We then determined the ability of each primer pair to detect immature parasitoids inside their aphid host. Detection was earlier for 16S than for LWRh, with parasitoids detected, respectively, 24 and 48 h after egg injection. Finally, we applied this method to assess parasitism rate in field populations of several aphid species. The interest of this tool for analysing aphid‐parasitoid food webs is discussed.

Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes

Aphidiinae are mostly composed of specialist parasitoids and the few species described as generalist are suspected to be composed of cryptic specialists, almost indistinguishable based on morphological characteristics. The use of molecular markers has proven to be a useful tool for revealing cryptic species complexes and here we use seven mitochondrial and nuclear gene fragments to study possible genetic differentiation among seven Aphidiinae generalists. Maximum likelihood (ML) trees and Bayesian Poisson tree processes (bPTP) models were conducted on each gene separately and on the seven genes together. The standard cytochrome c oxidase I barcode region appeared to be the most polymorphic and probably the best marker to reveal putative cryptic species. However, we showed with ML trees and bPTP models that a complementary use of mitochondrial and nuclear genes was the most relevant approach to reliably identify cryptic genetic clades in the Aphidiinae. Overall, most of the analysed generalist morphospecies were shown to be composed of subgroups related to the aphid host, some of them revealed as cryptic species by the species delimitation analysis. Further studies are needed to reveal the generality of this result in Aphidiinae.

Selecting volatiles to protect brassicaceous crops against the cabbage root fly, Delia radicum

Volatiles resulting from plant–herbivore interactions play an important role in the behavioral decisions of phytophagous, predatory, and parasitoid insects and could be used for managing pest insects. However, to date and after about 40 years of research, documented studies on applications in the field remain extremely scarce. Delia radicum L. (Diptera: Anthomyiidae), the cabbage root fly, is a major pest of brassicaceous crops for which classical control strategies are currently lacking. Our previous studies showed that dimethyl disulfide (DMDS), a compound emitted by roots heavily infested by D. radicum larvae, was attractive for the fly’s main natural enemies and could lead to a reduction of 60% in number of eggs laid on treated plants in the field. As a follow‐up of this work, we conducted another field study to select additional volatiles that could be used in a push–pull approach. Several synthetic herbivore‐induced plant volatiles, selected on the basis of their potential action on the behavior of both the fly and its natural enemies, were placed in odor dispensers in experimental broccoli plots and their influence on oviposition by D. radicum and egg predation by ground‐dwelling predators was assessed. Our results confirmed the role of DMDS in reducing D. radicum egg numbers on broccoli plants and revealed that (Z)‐3‐hexenyl acetate, a green leaf volatile released by recently damaged plants, strongly stimulated fly oviposition. Also, two of the compounds tested slightly modified predation activity of ground‐dwelling predators: acetophenone decreased the proportion of predated patches, whereas methyl salicylate increased it. This study is a first step in designing a push–pull strategy to control the cabbage root fly.

Oviposition Behavior of the Pollen Beetle (Meligethes aeneus): A Functional Study

The recognition by female phytophagous insects of a plant as a ‘good’ or ‘bad’ host for egg laying is based on a variety of cues (either visual, physical or chemical). Specific cues are often looked for during stereotypic oviposition behaviors, composed of several phases having their own function(s). In this study the oviposition behavior of the pollen beetle Meligethes aeneus, a pest which lays eggs in flower buds of only some brassicaceous plants, was described in detail on five oilseed rape (Brassica napus) genotypes. In parallel, setae borne by the ovipositor were characterized by scanning electron microscopy. Observations showed that the stereotypic oviposition sequence is functionally divided into three independent phases: external inspection, internal inspection and egg laying. The ovipositor plays a role in all phases by gaining information about external and internal bud parts. This role appears to be only physical since all the setae it bears are mechanoreceptors. Despite the fact that the pollen beetle is a specialist for oviposition, important variations in secondary metabolites that are typical of its host plant family (i.e., glucosinolates) on the bud did not influence clutch size. The crucial phase in the oviposition sequence seems to be the external inspection, during which poor and high-quality host plants are probably discriminated. Chemical information on bud surface is likely to be determinant in this process.

Larval Hitch-Hiking and Adult Flight are Two Ways of Aphidiinae Parasitoids Long-Range Dispersal

ABSTRACT Dispersal strategies and success of pests’ natural enemies widely influence the efficiency of biological control. In this study, we compare two dispersal strategies among Aphidiinae parasitoids: eggs and larvae dispersal through winged aphid flight and active dispersal by adult parasitoids. Using a molecular method applied to a sample of >2,000 winged migratory aphids captured in a suction trap situated in Western France, we assessed the proportion of winged aphids carrying an aphidiine larva. In the six most abundant aphid species, we found an average parasitism rate of migrating aphids close to 1% and identified seven different, mainly generalist, parasitoid species. We also identified the species and the sex of adult Aphidiinae captured by the suction trap based on morphological criteria. We found that dispersing adult parasitoids were almost exclusively female. Parasitoid dispersal strategy seems to be species-dependant but this result needs to be confirmed by an exhaustive analysis of winged aphids captured. We discuss the possible impact of the low parasitism rate of winged aphids on parasitoid population dynamics and the importance of these results in the context of biological control and of the study of food webs between aphids and their natural enemies.