Parasitoid-mediated indirect interactions between unsuitable and suitable hosts generate apparent predation in microcosm and modeling studies

Lucie S. Monticelli, Nicolas Desneux, George E. Heimpel

Research output: Contribution to journalArticlepeer-review

Abstract

Parasitoids used as biological control agents often parasitize more than a single host species and these hosts tend to vary in suitability for offspring development. The population dynamics of parasitoids and hosts may be altered by these interactions, with outcomes dependent on the levels of suitability and acceptance of both host species. Parasitism of individuals of an unsuitable host species may indirectly increase populations of a suitable host species if eggs laid into unsuitable hosts do not develop into adult parasitoids. In this case, the unsuitable host is acting as an egg sink for parasitoids and this can reduce parasitism of suitable hosts under conditions of egg limitation. We studied parasitoid-mediated indirect interactions between two aphid hosts, Aphis glycines (the soybean aphid) and A. nerii (the milkweed, or oleander aphid), sharing the parasitoid Aphelinus certus. While both of these aphid species are accepted by A. certus, soybean aphid is a much more suitable host than milkweed aphid is. We observed a drastic reduction of parasitoid offspring production (45%) on the suitable host in the presence of the unsuitable host in microcosm assays. Aphelinus certus females laid eggs into the unsuitable hosts (Aphis nerii) in the presence of the suitable host leading to egg and/or time limitation and reduced fitness. The impact of these interactions on the equilibrium population sizes of the three interacting species was analyzed using a consumer–resource modeling approach. Both the results from the laboratory experiment and the modeling approaches identified apparent predation between soybean aphid and milkweed aphid, in which milkweed aphid acts as a sink for parasitoid eggs leading to an increase in the soybean aphid population. The presence of soybean aphids had the opposite effect on milkweed aphid populations as it supported increases in parasitoid abundance and thus reduced the fitness and abundance of this aphid species.

Original languageEnglish (US)
Pages (from-to)2449-2460
Number of pages12
JournalEcology and Evolution
Volume11
Issue number6
DOIs
StatePublished - Mar 2021

Bibliographical note

Funding Information:
We thank Jonathan Dregni for technical assistance. This research was supported by a grant from the Marie‐Curie F7‐IRSES Action to ND (APHIWEB project, grant number: 611810) and a PhD fellowship from the Doctoral School Sciences de la Vie et de la Santé ED85 to LSM, and by support of the North Central Soybean Research Program, the Minnesota Soybean Research and Promotion Council, the University of Minnesota Rapid Agricultural Response Fund, the University of Minnesota Agricultural Experiment Station and an award to GEH from the Minnesota Invasive Terrestrial Plants and Pests Center. We also thank two anonymous reviewers for insightful comments on a previous version of this ms.

Publisher Copyright:
© 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Keywords

  • Aphelinus certus
  • Aphis glycines
  • Aphis nerii
  • apparent parasitism
  • apparent predation
  • biological control
  • egg sink
  • evolutionary trap

PubMed: MeSH publication types

  • Journal Article

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