Andrea Lucchi

Chemical Ecology and Management of Lobesia botrana (Lepidoptera: Tortricidae)

ABSTRACT The moth Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae) feeds on grapes (Vitis vinifera L.), reducing yield and increasing susceptibility to fungal infections. L. botrana is among the most economically important insects in Europe and has recently been found in vineyards in Chile, Argentina, and California. Here, we review L. botrana biology and behavior in relation to its larval host (the grapevine) and its natural enemies. We also discuss current and future control strategies in light of our knowledge of chemical ecology, with an emphasis on the use of the sex pheromone-based strategies as an environmentally safe management approach. Pheromone-mediated mating disruption is the most promising technique available on grapes and is currently implemented on ≈140,000 ha in Europe. Experience from several growing areas confirms the importance of collaboration between research, extension, growers, and pheromone-supply companies for the successful implementation of the mating disruption technique. In the vineyards where mating disruption has been successfully applied as an areawide strategy, the reduction in insecticide use has improved the quality of life for growers, consumers, as well as the public living near wine-growing areas and has thereby reduced the conflict between agricultural and urban communities.

Disruption of the reproductive behaviour of Scaphoideus titanus by playback of vibrational signals

Scaphoideus titanus Ball (Hemiptera: Cicadellidae: Deltocephalinae) is the vector of the grapevine disease Flavescence dorée. In S. titanus the male–female duet (MFD), based on species‐specific vibrational signals, is essential for successful copulation. The female reply within a duet is a single pulse that is coupled with the male pulse with constant latency. It has been shown that a rival male can interrupt an existing duet by emitting disruptive noise signals. We tested whether the reproductive behaviour of S. titanus can be disrupted by the playback of intra‐specific and synthesized vibrational signals. Tested males responded to the playback of an MFD with typical rivalry behaviour. Such behaviour includes silent search for a duetting female (satellite behaviour) and/or emission of disruptive signals. These signals were emitted either after exchange of male–female pulses or after two male pulses coupled by latency corresponding to the female response window. The onset of male disruptive signals overlapped with a female pulse. We suggest that the intruder’s disruptive signals can mask the female reply and confuse courting males. Playback of disruptive vibrational signals reduced the level of male calling and interrupted an established MFD that consequently resulted in a significantly reduced number of copulations. These results indicate that the vibrational communication channel is open to interference either from abiotic environmental noise or from signals produced by sexual competitors or heterospecifics. The present study also suggests that a detailed understanding of leafhopper behaviour is essential for trying new approaches in the development of more environmentally friendly control practices.

Synthetic Grape Volatiles Attract Mated Lobesia botrana Females in Laboratory and Field Bioassays

In laboratory experiments, we identified and quantified volatiles emitted by inflorescences and berries of two grape varieties (Trebbiano and Sangiovese) and examined the effects of the volatiles on oviposition by the grapevine moth Lobesia botrana. Compared to Trebbiano, Sangiovese is relatively more susceptible to L. botrana infestations under natural conditions. Chemical and electrophysiological analysis indicated only quantitative differences between the volatiles released by the two varieties. In a dual-choice oviposition bioassay based only on volatile cues, females did not show any preference between the two varieties. The six major components of the odor profiles that were GC-EAD-active to female antennae included: limonene, 4,8-dimethyl-1,(E)-3,7-nonatriene, (±)-linalool, (E)-caryophyllene, (E,E)-α-farnesene, and methyl salicylate. At the beginning of the berry touch phenological stage, their proportions were about 10:0.6:0.4:0.5:0.9:0.6 in Trebbiano and 10:1:0.4:1.5:0.4:0.3 in Sangiovese. A six-component synthetic lure (with the proportion 10:1:1:1:1:1, which approximated the ratio of components released by both varieties) was used in further laboratory oviposition bioassays. Depending on its dosage, the synthetic lure either attracted or repelled oviposition. L. botrana females laid significantly more eggs in the presence of either the grape bunches or the synthetic lure at the attractive dosage. In a release-capture experiment conducted in a field cage that covered two grapevine rows, the synthetic lure was more attractive than a grape cluster or a blank control, and it stimulated oviposition on the vegetation near the lure. The results indicate that L. botrana uses olfactory cues to select oviposition sites and that an artificial lure, containing the major volatiles released by two grape varieties, may be useful in monitoring female activity in the field.

Exploitation of insect vibrational signals reveals a new method of pest management.

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.

Inter-Plant Vibrational Communication in a Leafhopper Insect

Vibrational communication is one of the least understood channels of communication. Most studies have focused on the role of substrate-borne signals in insect mating behavior, where a male and a female establish a stereotyped duet that enables partner recognition and localization. While the effective communication range of substrate-borne signals may be up to several meters, it is generally accepted that insect vibrational communication is limited to a continuous substrate. Until now, interplant communication in absence of physical contact between plants has never been demonstrated in a vibrational communicating insect. With a laser vibrometer we investigated transmission of natural and played back vibrational signals of a grapevine leafhopper, Scaphoideus titanus, when being transmitted between leaves of different cuttings without physical contact. Partners established a vibrational duet up to 6 cm gap width between leaves. Ablation of the antennae showed that antennal mechanoreceptors are not essential in detection of mating signals. Our results demonstrate for the first time that substrate discontinuity does not impose a limitation on communication range of vibrational signals. We also suggest that the behavioral response may depend on the signal intensity.

Oviposition response of the moth Lobesia botrana to sensory cues from a host plant

The grapevine moth Lobesia botrana is a generalist insect herbivore and grapevine is one of its hosts. Previous studies have shown that insects use their olfactory abilities to locate hosts from a distance; whereas contact chemoreception mediates the stimulation of oviposition after landing. Little is known about the role of olfaction and its interactions with contact chemoreception and vision once the insect lands on the plant. Plant volatile compounds can be sensed by host-searching insects located some distance from the plant and insects sense both volatile and nonvolatile cues after landing on a plant. In the present study, we investigated the effects of these volatile and nonvolatile cues on the oviposition behavior of L. botrana. A behavioral bioassay with choice was developed in which insects were offered each sensory cue either alone or in combination with one or 2 other cues. Females were allowed to choose between a device with the stimulus and a blank device. Results were evaluated in terms of 2 parameters: quantity of eggs laid (egg counts) and preference for the stimulus (ODI: oviposition discrimination index). Our results suggest that olfaction significantly affects egg quantity and that there is significant synergism between olfaction and vision, in terms of their combined effect on egg quantity. In terms of preference (ODI), our results did not show a significant preference for any single cue; the highest ODI was measured for the full-cue stimulus (olfaction, vision, and contact). For ODI, a significant interaction was observed between olfaction and vision and a nearly significant interaction was observed between the olfactory and contact cues. The results are discussed in relation to the effects of plant sensory cues on the oviposition behavior of L. botrana.

Manipulating behaviour with substrate‐borne vibrations – potential for insect pest control

This review presents an overview of the potential use of substrate-borne vibrations for the purpose of achieving insect pest control in the context of integrated pest management. Although the importance of mechanical vibrations in the life of insects has been fairly well established, the effect of substrate-borne vibrations has historically been understudied, in contrast to sound sensu stricto. Consequently, the idea of using substrate-borne vibrations for pest control is still in its infancy. This review therefore focuses on the theoretical background, using it to highlight potential applications in a field environment, and lists the few preliminary studies that have been or are being performed. Conceptual similarities to the use of sound, as well as limitations inherent in this approach, are also noted.

Mating Behavior of Hyalesthes obsoletus (Hemiptera: Cixiidae)

ABSTRACT The mating behavior of Hyalesthes obsoletus Signoret (Hemiptera: Cixiidae) was studied to determine the role of substrate-borne vibrational signals in partner recognition, pair formation, and courtship. Planthopper vibrational signals were detected from nettle, Urtica dioica L., cuttings by laser vibrometer. Either male or female could initiate the mating sequence that was divided into three sections: recognition, courtship and precopula. The females were the more vibrationally active gender in the recognition stage and males in the courtship and precopula stages. Four distinct syllables constituted the male repertoire and were emitted in different behavioral contexts. The male syllable 1 was used during the recognition duet, as a reply to female pulse trains and it formed, in combination with male syllable 4, the male precopula signal. This latter signal was emitted in the vicinity of a receptive female and accompanied by jerky lateral movements of the body and tapping of the legs to the substrate. Although nonduetting males emitted long trains composed of male syllable 2, males during the courtship phase emitted trains formed mainly by male syllable 3. Female vibrational signals consisted of pulses, emitted either in trains during the recognition phase or as single pulses, in reply to male trains in the courtship stage. In the precopula phase, the females ceased signaling. According to our results, in H. obsoletus the vibrational signals play a major role in stimulating the male search process and in ensuring the female acceptance.

Study on the Role of Olfaction in Host Plant Detection of Scaphoideus titanus (Hemiptera: Cicadellidae) Nymphs

ABSTRACT The American grapevine leafhopper, Scaphoideus titanus Ball (Hemiptera: Cicadellidae), is the vector of the phytoplasma that causes Flavescence dorée, one of the most threatening grapevine yellows disease. The role of olfaction in host plant detection of this species is still unknown. In this study, the attractiveness of a host plant, the grapevine rootstock Vitis riparia × rupestris 101/14, to nymphs was verified through behavioral bioassays in a vertical glass Y-olfactometer. Furthermore, the olfactory sensitivity to odors extracted from grapevine organs headspace and the external morphology of the antennae were studied by electroantennography (EAG) and scanning electron microscopy (SEM), respectively. Headspace collections were made from fresh apical shoots and leaves. Concentrated extracts were analyzed by coupled gas chromatography and mass spectrometry (GC-MS) to identify volatile compounds. In EAG experiments, weak responses to plant odors were recorded. SEM observations indicated the presence of few antennal sensilla, potentially associated with olfaction. Our results suggest that olfactory cues may play a role in the host plant detection of S. titanus nymphs.

Active Space and the Role of Amplitude in Plant-Borne Vibrational Communication

Unlike airborne signals, substrate-borne vibrational signals are confined within the size and shape of their medium of communication, which in the case of small arthropods often coincides with the host plant. By following the substrate continuity, a vibrational signal creates a more or less complex active space network that enables communication between individuals. Due to the heterogeneity of plants, physical properties of the substrate can vary in the efficiency of signal transmission and in the diffusion of signals along the tissues. Under such circumstances, the identification and location of a potential partner may be a difficult task. Amplitude cues can be of great importance in orientation to the source of a vibrational signal by providing information about both direction and distance. As examples, we present two case studies on mating behavior of a leafhopper and a planthopper.