Research Article: Ubiquitous Water-Soluble Molecules in Aquatic Plant Exudates Determine Specific Insect Attraction

Date Published: October 8, 2008

Publisher: Public Library of Science

Author(s): Julien Sérandour, Stéphane Reynaud, John Willison, Joëlle Patouraux, Thierry Gaude, Patrick Ravanel, Guy Lempérière, Muriel Raveton, Tom Pizzari.

Abstract: Plants produce semio-chemicals that directly influence insect attraction and/or repulsion. Generally, this attraction is closely associated with herbivory and has been studied mainly under atmospheric conditions. On the other hand, the relationship between aquatic plants and insects has been little studied. To determine whether the roots of aquatic macrophytes release attractive chemical mixtures into the water, we studied the behaviour of mosquito larvae using olfactory experiments with root exudates. After testing the attraction on Culex and Aedes mosquito larvae, we chose to work with Coquillettidia species, which have a complex behaviour in nature and need to be attached to plant roots in order to obtain oxygen. This relationship is non-destructive and can be described as commensal behaviour. Commonly found compounds seemed to be involved in insect attraction since root exudates from different plants were all attractive. Moreover, chemical analysis allowed us to identify a certain number of commonly found, highly water-soluble, low-molecular-weight compounds, several of which (glycerol, uracil, thymine, uridine, thymidine) were able to induce attraction when tested individually but at concentrations substantially higher than those found in nature. However, our principal findings demonstrated that these compounds appeared to act synergistically, since a mixture of these five compounds attracted larvae at natural concentrations (0.7 nM glycerol, <0.5 nM uracil, 0.6 nM thymine, 2.8 nM uridine, 86 nM thymidine), much lower than those found for each compound tested individually. These results provide strong evidence that a mixture of polyols (glycerol), pyrimidines (uracil, thymine), and nucleosides (uridine, thymidine) functions as an efficient attractive signal in nature for Coquillettidia larvae. We therefore show for the first time, that such commonly found compounds may play an important role in plant-insect relationships in aquatic eco-systems.

Partial Text: Plant attractiveness to insects has been widely studied in plant-herbivore-parasitoid interactions. Volatile Organic Compounds (VOCs) emitted by plant–herbivore interactions are of importance for host or prey location by parasitoids and predators of phytophagous insects [1]–[6]. Some plants are able to release volatile infochemicals during an attack by specific herbivorous insects that attract predators specialized on the herbivore species. These predators respond to these chemical signals by attacking the herbivores, thereby reducing the plant’s tissue loss by herbivory [7]–[8]. More than 1000 VOCs are involved in such interactions [9], and in a single plant–herbivore complex 30–50 VOCs are frequently detected by chromatographic (GC-MS) analysis [6]. Among the wide variety of attractive compounds for terrestrial insects, the majority are represented by species-specific chemicals, mainly produced by plant secondary metabolism, such as polyphenols, isothiocyanates, terpenoids, fatty acid derivatives, benzoids and nitrogen or sulfur containing compounds [9], [10]–[11]. Ubiquitous metabolites such as alcohols or sugars have been shown to be involved in such interactions, but it seems that they act as phagostimulants [12]. It has been suggested that not only is the composition of the plant signal important in the insect attractiveness by plant, but also the proportion of the different VOCs presents in the emitting signal [13]. It has been demonstrated that plants emit distinct volatile blends in response to two closely related herbivore species, and that the parasitoids are able to distinguish these two signals suggesting a sophisticated chemical system of plant-herbivore-parasitoid interaction [14].

Our initial working hypothesis was that the relationship between Coquillettidia and aquatic macrophytes, which is unusual among plant-insect interactions since it is non-destructive [37]–[39], was mediated by plant release of very specific compounds. However, our study clearly demonstrates that widespread plant molecules, at very low concentrations, were responsible for this interaction. For the first time in an aquatic environment, we demonstrate that a synergism between the different attractive compounds present in the emitted signal occurred in this particular plant–insect interaction.