Untangling the aphid-parasitoid food web in citrus: Can hyperparasitoids disrupt biological control?

Abstract

Molecular techniques are irreplaceable to untangle the trophic links in communities where immature entomophagous species (either in the third or fourth level) develop inside the phytophagous. This is the case of aphid-parasitoid communities. Here, we develop a DNA-based approach to untangle the structure of the aphid-parasitoid food web in citrus, where Aphis spiraecola Patch. (Hemiptera: Aphididae) is a key pest and Binodoxys angelicae Haliday (Hymenoptera: Braconidae), its dominant primary parasitoid, is attacked by a complex of hyperparasitoids. Aphid populations and parasitism were followed at weekly intervals in 2012 and 2013. Parasitism rates were low (∼0.04 in the four sampled orchards). Simultaneously, colonies harboring aphid mummies were collected. Approximately half of the mummies were reared to adulthood and at least six hymenopteran hyperparasitoid species were identified by classical means: Syrphophagus aphidivorus (Mayr) (Encyrtidae), Alloxysta sp. (Forster) (Figitidae), Asaphes sp. (Walker) (Pteromalidae), Pachyneuron aphidis (Bouché) (Pteromalidae), Dendrocerus sp. (Ratzeburg) (Megaspilidae) and Phaenoglyphis villosa (Hartig) (Figitidae). The other half was subjected to a Taqman-based multiplex PCR to investigate trophic relationships in this food web. We confirmed that all six species hyperparasitized B. angelicae. The most abundant hyperparasitoids were S. aphidivorus and Alloxysta sp. Both were abundant from the beginning of the season, and hyperparasitism rates remained high (∼0.4) throughout the season in the two study years. Although these species could share the same mummy, S. aphidivorus and Alloxysta sp. were the most abundant species and dominated this food web. Finally, hyperparasitoids also increased the secondary sex ratio of B. angelicae. Thus, hyperparasitism probably explains the low impact of B. angelicae on A. spiraecola populations.