Elevated CO₂ Concentrations Impact the Semiochemistry of Aphid Honeydew without Having a Cascade Effect on an Aphid Predator

Abstract

Honeydew is considered a cornerstone of the interactions between aphids and their natural enemies. Bacteria activity occurring in aphid honeydew typically results in the release of volatile organic compounds (VOCs) that are used by the natural enemies of aphids to locate their prey. Because atmospheric carbon dioxide (CO₂) concentration directly impacts the physiology of plants, we raise the hypothesis that elevated CO₂ concentrations impact the quantity of honeydew produced by aphids, as well as the diversity and quantity of honeydew VOCs, leading to cascade effects on the foraging behavior of aphids' natural enemies. Using solid-phase microextraction, we analyzed the VOCs emitted by honeydew from pea aphids (Acyrthosiphon pisum Harris) reared under 450 ± 50 ppm of CO₂ (aCO₂) or 800 ± 50 ppm CO₂ (eCO₂). While the total amount of honeydew excreted was only slightly reduced by eCO₂ concentrations, we detected qualitative and quantitative differences in the semiochemistry of aphid honeydew between CO₂ conditions. Three VOCs were not found in the honeydew of eCO₂ aphids: 3-methyl-2-buten-1-ol, 2-methyl-1-butanol, and isobutanol. However, no difference was observed in the searching and oviposition behaviors of hoverfly (Episyrphus balteatus (De Geer)) females exposed to plants covered with honeydew originating from the different CO₂ conditions. The present work showed the effect of a particular aspect of atmospheric changes, and should be extended to other abiotic parameters, such as temperature.

Keywords: Acyrthosiphon pisum; Episyrphus balteatus; carbon dioxide; climate change; honeydew production; searching behavior; volatile organic compounds.

Figure 1

Amount (ng ± standard error (SE)) of the different volatile organic compounds (VOCs) emitted by the honeydew of A. pisum reared under aCO₂ (white bars) and eCO₂ (grey bars) conditions.

Figure 2

Percentage of time (±SE) that hoverfly females expressed different behaviors on plants smeared with crude honeydew from aCO₂ (white bars) and eCO₂ (grey bars) conditions in a dual-choice assay. The random choice category (black bar) was shared for both CO₂ conditions.

Figure 3

Mean (±SE) number of eggs laid by the hoverfly females on plants smeared with crude honeydew from aCO₂ (white bars) and eCO₂ (grey bars) conditions.