An Experimental Test of the Adaptive Host Manipulation Hypothesis: Altered Microhabitat Selection in Parasitized Pea Aphids

The behavioral phenotypes of hosts may be altered during parasitism, which could favor either the host or the parasite. Pea aphid Acyrthosiphon pisum hosts parasitized by the primary parasitoid wasp Aphidius ervi leave the stems or lower leaf surfaces where they are most commonly found and move to upper leaf surfaces before they die and mummify. In order to test whether the change of microhabitat benefits the host or the parasitoid, we transplanted pea aphid mummies reared in the laboratory to three different microhabitats on alfalfa plants in the field: the upper leaf surfaces, the lower leaf surfaces, and the stems. Survival analysis revealed no significant differences in mummy survival to emergence across the microhabitat treatments before an alfalfa harvest, when predation pressure was very high, and 2 weeks after an alfalfa harvest, when predation pressure was very low. In contrast, 5 weeks after an alfalfa harvest, when predation pressure was intermediate differences in predation risk were apparent: mummies transplanted to the upper leaf surface had the lowest mortality rates, mummies transplanted to the lower surface of leaves had intermediate mortality rates, and mummies transplanted to the stems had the highest mortality rates. Furthermore, a laboratory study suggested that, compared to other plant substrates, mummies on stems were more likely to be preyed upon by the ladybeetle, Hippodamia convergens, which concentrated its search on stems. Our results support the adaptive manipulation hypothesis, in that parasitized aphids appear to induce their host to move to a region of reduced predator foraging, where their risk of attack is reduced.