An ant-coccid mutualism affects the behavior of the parasitoid Aenasius bambawalei, but not that of the ghost ant Tetramorium bicarinatum

Jun Huang,Peng-Jun Zhang,Juan Zhang,Ya-Yuan Tang

doi:10.1038/s41598-017-05442-6

Abstract

Mutualisms between honeydew-producing insects and ants change the emission of volatiles from plants, but whether such changes alter the behaviors of ants that tend honeydew-producing insects or wasps that parasitize honeydew-producing insects remain unknown. This study compared the behavioral responses of the ant Tetramorium bicarinatum and the parasitoid wasp Aenasius bambawalei to odors from cotton plants infested with the mealybug Phenacoccus solenopsis or infested with the mealybug and the ant, which tends the mealybug. The ant could not distinguish between the volatiles from plants infested with the mealybug alone and those from plants infested with the mealybug and the ant. Likewise, naïve wasps failed to distinguish between volatiles from the two treatments. In contrast, experienced wasps preferred volatiles from plants infested with the mealybug and the ant. Volatile analysis showed that the amounts of MeSA were increased and those of methyl nicotinate were decreased when plants were infested by the mealybug and the ant rather than when plants were uninfested or were infested by the mealybug alone. Thus, the mutualism between the mealybug and ant changed the volatiles emitted by cotton plants such that the attraction of A. bambawalei (but not that of the ant) to the plants was increased.

Highlights

Based on most previous studies, protection occurs because tending ants directly attack parasitoids and cause parasitoids to take evasive action[8,9,10]
We attempted to answer the following questions: (1) Do ant-tended mealybug colonies affect the olfactory response of A. bambawalei and does the response of A. bambawalei change with experience? (2) Does mealybug infestation (=mealybug injury or damage) induce ant recruitment to plants in the absence of mealybug encounters? and (3) Does mealybug infestation change the volatile compounds emitted by cotton plants? To identify the compounds that changed with the infestation and to identify those linked to ant tending, we sampled volatiles emitted by cotton plants alone and those infested with the mealybug with or without the ghost ant
Pairs of plants were used in an olfactometer assay with experienced or inexperienced A. bambawalei females, i.e., with females that had or had not been exposed to volatiles from plants infested with mealybugs and ants

Summary

Introduction

Based on most previous studies, protection occurs because tending ants directly attack parasitoids and cause parasitoids to take evasive action[8,9,10]. We hypothesized that the damage caused by the mealybugs will change the volatile compounds and induce rapid ant recruitment or continuous ant patrols of leaves until mealybugs are encountered. To test these two hypotheses, we chose a mutualism on cotton plants that consisted of the cotton mealybug Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) and the tending ghost ant Tetramorium bicarinatum (Hymenoptera: Formicidae), which is one of the most widely distributed ant species worldwide[17]. Aenasius bambawalei (Hymenoptera: Encyrtidae) is a primary parasitoid of the mealybug[20], and the parasitism rate in the field can exceed 62%21 This system is suitable for examining interactions between the mealybug, the tending ant, and the parasitoid wasp. We attempted to answer the following questions: (1) Do ant-tended mealybug colonies affect the olfactory response of A. bambawalei and does the response of A. bambawalei change with experience? (2) Does mealybug infestation (=mealybug injury or damage) induce ant recruitment to plants in the absence of mealybug encounters? and (3) Does mealybug infestation change the volatile compounds emitted by cotton plants? To identify the compounds that changed with the infestation and to identify those linked to ant tending, we sampled volatiles emitted by cotton plants alone and those infested with the mealybug with or without the ghost ant

Methods

Results

Conclusion