Modification of Herbivore and Parasitoid Behavior Over Three Trophic Levels by the Entomopathogen Nosema pyrausta (Microsporida: Nosematidae)

Abstract

Effects of the microsporidian Nosema pyrausta Paillot on behavior of the European corn borer, Ostrinia nubilalis (Hubner), and its parasitoid, Macrocentrus grandii Goidanich, were examined in the laboratory. Silk produced by O. nubilalis larvae around feeding and pupation sites was more frequently diffuse (cobweblike, unstructured) in diet cups containing N. pyrausta -infected larvae; however, frequency of diffuse silk production by O. nubilalis larvae was not influenced by M. grandii parasitism. We found no evidence of N. pyrausta spores in the silk produced by infected O. nubilalis larvae. Three O. nubilalis cocoon statuses were identified as follows: (1) complete cocoon, in which thick silk cocoon completely surrounded larvae or larval remains at O. nubilalis or M. grandii pupation; (2) incomplete cocoon, which was open on one or more sides at pupation; and (3) no cocoon at pupation. The percentage of O. nubilalis larvae that formed a complete cocoon or no cocoon was significantly influenced by both infection by N. pyrausta and parasitism by M. grandii. O. nubilalis larvae that had been either infected or parasitized displayed ≈7.2- and 12.3-fold increases in activity, respectively. Larvae that had been both infected and parasitized displayed a 45-fold increase in level of activity. Sixty-two to 80% of parasitoids emerging from hosts with an incomplete cocoon, and >91% emerging from no cocoon, were unable to spin their own cocoons, wandered from host carcasses, and did not pupate. The incidence of M. grandii spinning and wandering, and distance wandered, were independent of N. pyrausta dosage to which host larvae were exposed. Fully fed M. grandii larvae, which emerged from hosts that had not spun cocoons and were placed in complete cocoons, were able to pupate successfully and to emerge, regardless of infection status.