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Periodic Report Summary 1 - APHIWEB (Structure, strength and invasibility of aphid food webs)

APHIWEB: summary of the project and expected results:
The project addresses the changes in food web structure and function resulting from emigration / invasion of some of the representative of lower trophic levels (herbivores) and of their natural enemies, from their origin centre to invaded regions. Migration of a given herbivore species may release it from predation pressure as stated in the enemy release hypothesis. For agricultural pests, such enemy release could result in major pest outbreaks. Conversely, increased natural enemy pressure could occur if pest enemies are ‘freed’ from the restraints imposed by upper trophic levels after migration, e.g. fewer or no hyperparasitoids. The work will shed light on the resilience or disruption of trophic interactions within a multi-level food web after migration (of pest) or importation events (release of natural enemies in framework of classical biocontrol programs). Results will also be valuable in application contexts: they would increase our ability to predict how food webs can respond to disturbances, e.g. species invasions in general, as well as depicting the reasons for success or failure of past and future introductions of exotic biocontrol agents. This project focuses on invasive aphid pests, their associated natural enemies (mainly parasitoids and predators) and the consumers of the latter (such as hyperparasitoids) in 6 plant systems distributed worldwide: oilseed rape, wheat, Citrus trees, soybean, Tansy plant and the complex Nerium oleander/Asclepias plants. Aphids cause multiple negative effects on crops, e.g. by feeding on plant sap (phloem) and by transmitting viruses, hence they represent a threat to these crops worldwide. The pest status of aphids (on the considered crops) differs across the world: they are major pests in invaded regions but often minor pests in their native region. This could account for the lower number of natural enemy species and the simpler food webs observed in native areas and thus explain the higher impact of those pests in invaded areas.
We are characterizing food webs including natural enemies of pest aphids, e.g. parasitoids and hyperparasitoids associated with aphids (and other insects associated with aphids, e.g. ants), in their native regions, and to compare them to remote sites where these agricultural or natural ecosystems and their aphid pests also occur such as invaded areas in various regions of the world. For each ecosystem, sites include the native area of the plant/crop and of aphid pest(s) and multiple regions across the world that have been invaded by the aphid(s) (and where natural enemies were or were not released). It will include countries in Europe, North and South Americas, Asia, and more isolated areas such as New Zealand and smaller islands. By considering food webs associated with pest insects and comparing food web structure and functioning on an international scale, we will broaden our understanding of processes underpinning food web functioning and herbivore population regulation. Comparison of food webs in various regions, both native & invaded ones, also focuses on factors structuring trophic networks associated with aphid pests in various ecosystems worldwide. To unravel the food web interactions, we use complimentary techniques.

Work packages:
WP1 Multidisciplinary characterization of aphids, natural enemies and intraguild consumers
WP2 Investigate the existing functional biodiversity in contrasted natural or agro-ecosystems
WP3 Food web construction, food web analysis and test of ecological theories at the food web level
WP4 Investigation of factors affecting success rates of introduction and/or invasion by aphid-associated natural enemies

Work progress: After 2 years of surveys and sample collections, we have been successful in getting enough data and samples (for further works) from native and invaded areas for the Citrus, Asclepias/Oleander and Wheat ecosystems; nearly 17,000 aphid mummies have been already collected so far. Further molecular work would be developed on these models. So far, no samples could be collected on soybean in the native area (China, owing to scarcity of aphids on soybean in this country) despite extensive sampling carried out throughout 2014-2015. Similar scarcity in tansy aphids, both in native and invaded areas, prevented the working groups to collect mummies in this ecosystem.
Molecular methods for assessing host-primary-parasitoid-hyperparasitoid trophic interactions as well as aphid/parasitoid-predator feeding interactions have been primarily developed for Central European wheat. These approaches are mostly based on diagnostic multiplex PCR allowing testing aphids and predators for DNA of parasitoids and aphids at different taxonomic levels (species, genus, group). Additionally, these approaches were combined with sequence-based identification of parasitoid DNA amplified from aphids to allow for identification of rare parasitoid species. So far these approaches have been applied to aphids collected in fields in Austria, Germany, Chile and China, and the methods are being transferred to partners across the APHIWEB network..
The factors modulating specialization of aphid parasitoids (host range) have been studied to document (i) how parasitoids introduced into a new area may attack encountered aphids, and (ii) how endemic parasitoids may attack exotic aphid species in the case of invasion.
When parasitoids are introduced in a new geographic region, genetic bottleneck may reduce their ability to attack and parasitize various hosts. This hypothesis was tested using the generalist parasitoid Lysiphlebus testaceipes which was introduced from America to Southern Europe 40 years ago. We demonstrated that the European population showed a different pattern of host suitability than the American population; this occurred both in terms of behavioral and physiological host ranges. In addition, physiological host range was related to genetic characteristics: crosses between the French and the American populations restored the typical physiological host range from the original population (American one).
Parasitoids' host range is usually seen as a static feature; however the physiological state of an individual may modify established patterns. We studied dynamic host specificity of parasitoids of aphids with two different life-histories (egg-limited and time-limited) under laboratory and greenhouse conditions, involving different aphid species commonly present as pests and natural enemies. Our results indicated that different physiological conditions can modify parasitoid host selection behavior. These behavior modifications may be adaptive for parasitiod species and may have consequences for their use in aphid pest management.
Honeydew, the sugar-rich source excreted by hemipterans (notably aphids), is the most dominant carbohydrates sources used by parasitoids; this might actually affect host use by parasitoids and ultimately parasitoid host range. Depending on the source of honeydew, the impact on parasitoid fitness (i.e. longevity and fecundity) can vary from negligible to substantial. Using various bioassay (notably anthrone), we demonstrated that the aphid honeydews (14 aphid species tested) increased the longevity and carbohydrate contents of L. testaceipes when compared with water. Finally, there was a positive correlation between honeydew suitability (parasitoid fitness) and the mean content of the three measured carbohydrates (fructose, “body sugars” and glycogen). These results have important implications for biological control because it shows that carbohydrate levels reveal not only the nutritional state of honeydew-fed parasitoids but also their fitness in the field.

Expected final results and their potential impact: The scope of potential results of the project is wide. Aphids being a worldwide pest, food web studies can provide crucial data for biological control applications, from classical to conservation approaches. The international scale of the study will enable investigating biogeographic hypotheses, which are a valuable contribution to ecological theory but are also applicable to biosecurity, e.g. safety of classical biological control programs for endemic biodiversity.

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Life Sciences
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