Exploitation of Insect Vibrational Signals Reveals a New Method of Pest Management

PLOS ONE, Dec 2019

Food production is considered to be the main source of human impact on the environment and the concerns about detrimental effects of pesticides on biodiversity and human health are likely to lead to an increasingly restricted use of chemicals in agriculture. Since the first successful field trial, pheromone based mating disruption enabled sustainable insect control, which resulted in reduced levels of pesticide use. Organic farming is one of the fastest growing segments of agriculture and with the continuously growing public concern about use of pesticides, the main remaining challenge in increasing the safety of the global food production is to identify appropriate alternative mating disruption approaches for the numerous insect pests that do not rely on chemical communication. In the present study, we show for the first time that effective mating disruption based on substrate-borne vibrational signals can be achieved in the field. When disruptive vibrational signals were applied to grapevine plants through a supporting wire, mating frequency of the leafhopper pest Scaphoideus titanus dropped to 9 % in semi-field conditions and to 4 % in a mature vineyard. The underlying mechanism of this environmentally friendly pest-control tactic is a masking of the vibrational signals used in mate recognition and location. Because vibrational communication is widespread in insects, mating disruption using substrate vibrations can transform many open field and greenhouse based farming systems.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0032954&type=printable

Exploitation of Insect Vibrational Signals Reveals a New Method of Pest Management

et al. (2012) Exploitation of Insect Vibrational Signals Reveals a New Method of Pest Management. PLoS ONE 7(3): e32954. doi:10.1371/journal.pone.0032954 Exploitation of Insect Vibrational Signals Reveals a New Method of Pest Management Anna Eriksson 0 Gianfranco Anfora 0 Andrea Lucchi 0 Francesco Lanzo 0 Meta Virant-Doberlet 0 Valerio Mazzoni 0 Guy Smagghe, Ghent University, Belgium 0 1 The Istituto Agrario di San Michele all'Adige Research and Innovation Centre, Fondazione Edmund Mach , San Michele all'Adige , Italy , 2 Department C.D.S.L., Section of Agricultural Entomology, University of Pisa , Pisa , Italy , 3 Department of Entomology, National Institute of Biology , Ljubljana , Slovenia Food production is considered to be the main source of human impact on the environment and the concerns about detrimental effects of pesticides on biodiversity and human health are likely to lead to an increasingly restricted use of chemicals in agriculture. Since the first successful field trial, pheromone based mating disruption enabled sustainable insect control, which resulted in reduced levels of pesticide use. Organic farming is one of the fastest growing segments of agriculture and with the continuously growing public concern about use of pesticides, the main remaining challenge in increasing the safety of the global food production is to identify appropriate alternative mating disruption approaches for the numerous insect pests that do not rely on chemical communication. In the present study, we show for the first time that effective mating disruption based on substrate-borne vibrational signals can be achieved in the field. When disruptive vibrational signals were applied to grapevine plants through a supporting wire, mating frequency of the leafhopper pest Scaphoideus titanus dropped to 9 % in semi-field conditions and to 4 % in a mature vineyard. The underlying mechanism of this environmentally friendly pest-control tactic is a masking of the vibrational signals used in mate recognition and location. Because vibrational communication is widespread in insects, mating disruption using substrate vibrations can transform many open field and greenhouse based farming systems. - Funding: This research was supported by the Autonomous Province of Trento (Accordo di Programma 2010), Funding Research Programme P1-0255 and Research Project V4-0525 by Slovenian Research Agency, Fondi Ateneo of Pisa University, and CBCEurope Ltd. (Milano, Italy). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors received funding from a commercial source (CBC-Europe Ltd.). This does not alter the authors adherence to all the PLoS ONE policies on sharing data and materials. For many insects, species-specific sex pheromones are essential in bringing together potential partners [1] and an early realization of the potential for exploiting chemical signals for pest control has led to a plethora of research and application through the last 50 years [2-4]. Today disruption of chemical communication is an integral part of pest management in several important crops worldwide [3-5]. However, numerous major insect pests do not rely on long-range chemical communication, most notably leafhoppers and planthoppers [6-8] that comprise more than 30,000 species [9-10]. In these insects mate recognition and localization of the partner are mediated exclusively via substrateborne vibrational signals [11] and their populations are currently managed primarily by insecticide treatments. Surprisingly, although males use special species-specific disruptive vibrational signals to interfere with the courtship of rivals [12-13], mating interruption by induced vibrations has been rarely considered even from a theoretical viewpoint and there has been virtually no research on how to exploit this common insect communication channel [14] as a tool for pest control [4,15]. Here we present the first implementation of mating disruption based on substrate-borne vibrations. The leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae), a vector of a lethal grapevine disease Flavescence doree, was chosen as a model pest species. In Europe Flavescence doree is a quarantine disease and compulsory measures to manage vector populations and prevent the spread of the disease include large-scale insecticide treatments [16]. In sexual communication of S. titanus a stable male-female vibrational duet is essential for successful localization of the female and, consequently, for copulation [13,14,17]. Because the initial step in pair formation of S. titanus is an emission of male calling signals [13,17], we first analyzed the velocity characteristics of these vibrational signals in semi-field conditions, by applying pre-recorded calls to one leaf of the grapevine plants that were later used for mating disruption tests. Next, we established whether disruptive vibrational (...truncated)


This is a preview of a remote PDF: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0032954&type=printable

Anna Eriksson, Gianfranco Anfora, Andrea Lucchi, Francesco Lanzo, Meta Virant-Doberlet, Valerio Mazzoni. Exploitation of Insect Vibrational Signals Reveals a New Method of Pest Management, PLOS ONE, 2012, Volume 7, Issue 3, DOI: 10.1371/journal.pone.0032954