Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?

PLoS One. 2020 Dec 16;15(12):e0242486. doi: 10.1371/journal.pone.0242486. eCollection 2020.

Abstract

Paper wasps (Polistes dominula), parasitized by the strepsipteran Xenos vesparum, are castrated and desert the colony to gather on plants where the parasite mates and releases primary larvae, thus completing its lifecycle. One of these plants is the trumpet creeper Campsis radicans: in a previous study the majority of all wasps collected from this plant were parasitized and focused their foraging activity on C. radicans buds. The unexpected prevalence and unusual feeding strategy prompted us to investigate the influence of this plant on wasp behavior and physiology through a multidisciplinary approach. First, in a series of laboratory bioassays, we observed that parasitized wasps spent more time than non-parasitized ones on fresh C. radicans buds, rich of extra-floral nectaries (EFNs), while the same wasps ignored treated buds that lacked nectar drops. Then, we described the structure and ultra-structure of EFNs secreting cells, compatible with the synthesis of phenolic compounds. Subsequently, we analysed extracts from different bud tissues by HPLC-DAD-MS and found that verbascoside was the most abundant bioactive molecule in those tissues rich in EFNs. Finally, we tested the immune-stimulant properties of verbascoside, as the biochemical nature of this compound indicates it might function as an antibacterial and antioxidant. We measured bacterial clearance in wasps, as a proxy for overall immune competence, and observed that it was enhanced after administration of verbascoside-even more so if the wasp was parasitized. We hypothesize that the parasite manipulates wasp behavior to preferentially feed on C. radicans EFNs, since the bioactive properties of verbascoside likely increase host survival and thus the parasite own fitness.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / isolation & purification
  • Anti-Bacterial Agents / pharmacology*
  • Bignoniaceae / parasitology
  • Chromatography, High Pressure Liquid
  • Feeding Behavior / drug effects
  • Glucosides / chemistry
  • Glucosides / isolation & purification
  • Glucosides / pharmacology*
  • Holometabola / physiology*
  • Host-Parasite Interactions*
  • Immunity, Innate / drug effects
  • Immunocompetence
  • Larva / physiology
  • Male
  • Mass Spectrometry / methods
  • Phenols / chemistry
  • Phenols / isolation & purification
  • Phenols / pharmacology*
  • Plant Nectar / chemistry
  • Wasps / drug effects
  • Wasps / immunology
  • Wasps / parasitology*

Substances

  • Anti-Bacterial Agents
  • Glucosides
  • Phenols
  • Plant Nectar
  • acteoside

Grants and funding

Financial support to LB was provided by the University of Florence.