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Behavioral manipulation (BM) is a multimodal control approach based on the interference with the stimuli mediating insect perception and interaction with the surroundings. BM could represent a win–win strategy for the management of vector-borne plant pathogens as the bacterium Xylella fastidiosa, since it could reduce the number of vectors alighting on host plants and, consequently, the chances for transmission to occur. In this review, we summarized current knowledge and highlighted gaps in information on (i) how insect vectors of X. fastidiosa in general, and more specifically the meadow spittlebug Philaenus spumarius, locate and accept the host plant; and (ii) how behavioral manipulation techniques could be applied to disrupt the vector–host plant interaction. Finally, we discussed how diverse BM strategies could be combined with other integrated pest management tools to protect olive groves from inoculation with the fastidious bacterium.

Halyomorpha halys (Stål, 1855), the brown marmorated stink bug (BMSB), is an invasive species that has become a key agricultural pest in its invaded range. Commercial traps available for BMSB monitoring rely on male produced aggregation pheromones as lure, with two possible shortcomings: trap spillover and low detection precision. In this study, we assessed if vibrational signals can increase the attractiveness of pheromone traps by testing the optimized vibration-based lure (Female Song 2, FS2) associated with a specifically designed trap (i.e., the vibrotrap). We evaluated the efficacy of this bimodal trap (i.e., pheromones + vibrations) on females, males and nymphs in controlled conditions (greenhouse) and in the field, in two sites at the margin of two commercial vineyards. In the field, bimodal vibrotraps were compared to three unimodal (i.e., only pheromone) trap types. Both experiments showed that the vibrotrap is highly attractive for BMSB, and the optimized FS2 signal significantly improved its effectiveness. Even though FS2 was selected to target males, the number of trapped females increased as well. Overall, the presented findings show a feasible improvement to future commercial BMSB traps through the synergic use of semiophysicals and semiochemicals. Further research is needed to evaluate the effectiveness of vibrotraps for both early detection and mass trapping.

Drosophila suzukii Matsumura is an economically important pest of small and stone fruits. Its establishment in the Americas and Europe marked an important turning point in crop management programs. Ten years after its first detection, an effective integrated pest management program has yet to be developed and pesticides are mainly used to control this pest. Here we test a new behavioral control tool, with the aim to develop an alternative pest control strategy. A food-grade gum matrix, was evaluated under controlled and open field conditions for its ability to attract the pest and protect the ripening fruit. Here, we report that the gum effectively reduces fruit infestation when used under managed conditions. We show that a single point source can affect D. suzukii behavior over a 3.6 m radius and last for up to 21 d. Open field data reveal that the efficacy of the gum is significantly impacted by water content. We discuss these results in respect to the future implications for D. suzukii management, along with important considerations on gum mechanism of action, possible application strategies and economic suitability for growers.

The increasing demand for safe and sustainably produced food is leading to the development of strategies of pest control alternative to chemicals. One innovative method is Vibrational Mating Disruption (VMD) to disrupt insect communication in plants. VMD was proven effective in preventing mating of the grapevine pest Scaphoideus titanus, vector of flavescence dorée. However, the stress induced by VMD on the target species has the potential to influence other crucial aspects of the insect biology and ethology. Therefore, the goal of this study was to understand side effects of VMD on the flight activity and oviposition of S. titanus. The results of our experiments conducted in the greenhouse showed that in the presence of a receptive female, males fly more if exposed to vibrations than in the silent control but not differently from singles males in silence. Surprisingly, we found that also females subjected to VMD fly more than in the silence. Regarding oviposition, we found that mated females exposed to vibrations and single females (unmated) laid significantly fewer eggs than mated females in silence. In conclusion, this study shows the potential of VMD to interfere, besides with mating, with other important biological aspects of the pest species.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) also known as spotted-wing drosophila (SWD), is a pest native to Southeast Asia. In the last few decades, the pest has expanded its range to affect all major European and American fruit production regions. SWD is a highly adaptive insect that is able to disperse, survive, and flourish under a range of environmental conditions. Infestation by SWD generates both direct and indirect economic impacts through yield losses, shorter shelf life of infested fruit, and increased production costs. Fresh markets, frozen berries, and fruit export programs have been impacted by the pest due to zero tolerance for fruit infestation. As SWD control programs rely heavily on insecticides, exceedance of maximum residue levels (MRLs) has also resulted in crop rejections. The economic impact of SWD has been particularly severe for organic operations, mainly due to the limited availability of effective insecticides. Integrated pest management (IPM) of SWD could significantly reduce chemical inputs but would require substantial changes to horticultural management practices. This review evaluates the most promising methods studied as part of an IPM strategy against SWD across the world. For each of the considered techniques, the effectiveness, impact, sustainability, and stage of development are discussed.

Insect societies require an effective communication system to coordinate members’ activities. Although eusocial species primarily use chemical communication to convey information to conspecifics, there is increasing evidence suggesting that vibroacoustic communication plays a significant role in the behavioural contexts of colony life. In this study, we sought to determine whether stridulation can convey information in ant societies. We tested three main hypotheses using the Mediterranean ant Crematogaster scutellaris: (i) stridulation informs about the emitter’caste; (ii) workers can modulate stridulation based on specific needs, such as communicating the profitability of a food resource, or (iii) behavioural contexts. We recorded the stridulations of individuals from the three castes, restrained on a substrate, and the signals emitted by foragers workers feeding on honey drops of various sizes. Signals emitted by workers and sexuates were quantitatively and qualitatively distinct as was stridulation emitted by workers on different honey drops. Comparing across the experimental setups, we demonstrated that signals emitted in different contexts (restraining vs feeding) differed in emission patterns as well as certain parameters (dominant frequency, amplitude, duration of chirp). Our findings suggest that vibrational signaling represents a flexible communication channel paralleling the well-known chemical communication system.

Biotremology is a field of study focused on an ancient way of communication by animals endowed with specialized organs for emission and reception of substrate-borne vibrations. Established as a scientific discipline of its own, formally separated from bioacoustics only recently, biotremology is now rapidly spreading throughout the scientific community, offering valuable cooperation also to numerous other scientific disciplines. Insects, make significant use of substrate-borne vibrational signals and cues for inter- and intraspecific communication, to accomplish many different behaviours. In this chapter, after highlighting the main relations, and differences, between insect acoustic and vibrational communication, we provide a detailed, comprehensive overview of the knowledge and ongoing research in the field of insect biotremology. We particularly emphasise the mechanisms of sensory detection of vibrational signals and cues, and the central neural processing of the received information; the latter especially being discussed in relation to insect auditory processing. In addition, we dedicate considerable attention to the behavioural and ecological aspects of insect vibrational communication, to the methods and instruments of research in neurophysiology and behavioural ecology, as well as the use of acquired basic knowledge in practical applications. Whilst some topics in biotremology, such as the neuronal basis of behaviour, need highly increased research attention, the interest in applied biotremology is rising especially quickly for the high potential offered by substrate-borne vibrations as semiophysicals for pest control. Hence, insects are both the elected study model for basic biotremology research and strongly relevant for agricultural and resource management issues.

BACKGROUND The glassy-winged sharpshooter (GWSS), Homalodisca vitripennis, is an important pest of grapevines due to its ability to transmit Xylella fastidiosa, the causal agent of Pierce's disease. GWSS mating communication is based on vibrational signals; therefore, vibrational mating disruption could be an alternative to insecticides for suppression of GWSS population. Our objectives were to identify spectral features of female signal that elicit male signaling, design disruptive signals able to alter male perception and acceptance of a female, and determine the signal intensity required for future field applications. RESULTS Results showed that male responses to playback of modified female signals were significantly reduced by 60-75%when part of the female signal spectral components above or below 400 Hz were deleted. Playback bioassays showed that transmission of an 80 Hz pure frequency tone to plants completely suppressed male signaling to female signal playback, even if the disruptive signal amplitude was 10 dB lower than the female signal playback. CONCLUSION Although the mechanism underlying cessation of male signaling activity in the presence of disruption is not yet understood, results suggest that an 80 Hz vibrational signal should be tested in laboratory and field experiments to assess its efficacy in disrupting mating of GWSS.

The recent description of a new vibrational mating disruption method to control the leafhopper Scaphoideus titanus Ball opened questions about its possible application to other leafhopper pests. Since the prerequisite for the method's successful application is a deep knowledge of the species mating behavior and the exact role of associated signals, we conducted behavioral assays on the green leafhopper Empoasca vitis Gothe, a pest of grapevine and other crops in Europe and Asia. Laser vibrometer recordings of single and paired individuals (male and female) during a 24-h period enabled us to detect and describe 2 male and 1 female signal. The pair formation starts when the female replies to a male call and a duet is established, then it continues through 2 different behavioral stages: Location and Courtship. The proper courtship begins only when the male locates the female. The latter is characterized by a significant change in temporal parameters that regards both the signals and the duet structure. Although the male calling activity and the female replying rate were the same during the 24 h, a lower number of matings was recorded during the night. We discuss the possible role of vision and of the species ecology as factors of reproductive success and mating strategy. Our conclusion is that the mechanical mating disruption technique seems feasible for future application to this species.

The glassy-winged sharpshooter (GWSS), Homalodisca vitripennis, is an important vector of Xylella fastidiosa, the causal agent of Pierce’s disease of grapevine. GWSS control relies mainly on insecticides; therefore, an alternative method, such as vibrational mating disruption, is required. However, knowledge of GWSS intraspecific communication is necessary to evaluate applicability of such methods. Mating behavior and associated vibrational signals were described in different social contexts: individuals, pairs, and one female with two competing males. Behavioral analysis showed that GWSS mating communication involved the emission of three male and two female signals, with specific roles in two distinct phases of mating behavior, identification and courtship. Mating success depended on vibrational duets between genders, which were temporarily interrupted in the presence of male rivalry. Male rivalry behavior involved the emission of three distinct rivalry signals. Two rivalry signals resemble female signals and were associated with replacement of the female in the duet by the rival male. The third rivalry signal was emitted by competing males. Data suggested that rival males used mimicry and hostile signals to interrupt the ongoing duet and gain access to a female. In the future, knowledge acquired from this study will be essential to develop a mechanical mating disruption method for GWSS control.

Drosophila suzukii (Matsumura) is a vinegar fly species that originates from Eastern Asia and has spread throughout Europe and the Americas since its initial detection in United States in 2008. Its relatively large, sclerotized, and serrated ovipositor enables the ability to penetrate ripening fruits, providing a protected environment for its egg and larval stages. Because the mechanism of oviposition site selection of D. suzukii is a matter of hypothesis, the aim of the present study was to elucidate behavioral and chemical aspects of short-range ovipositional site selection within the context of D. suzukii reproductive biology. The preference of D. suzukii to lay eggs on artificially pierced, previously infested, or intact fruits was tested. Video recordings and photographic evidence documented the release of an anal secretion over the fruit surface near the oviposition sites. Gas chromatographic analysis revealed the presence of 11 compounds detected only on the skin of egg-infested berries. Electroantennographic experiments with both sexes of D. suzukii highlighted the importance of six volatile compounds: methyl myristate, methyl palmitate, myristic acid, lauric acid, palmitic acid, and palmitoleic acid. Finally, a synthetic blend composed of the six compounds in a ratio similar to that found on the skin of egg-infested berries increased the oviposition rate of conspecific females. Data from our work suggest that the identified volatiles are cues for reproductive site selection. We discuss how these oviposition cues may affect the fitness of D. suzukii. The knowledge gained from this study may accelerate establishment of control strategies based on the interference and disruption of D. suzukii communication during the oviposition processes.

Until a few years ago, the concept of mating disruption had been exclusively associated with the use of pheromones to reduce population density of insect pests. Since the early 2000s, a novel approach has been proposed to the scientific community: vibrational mating disruption (VMD). The novelty is the use of disturbance vibrations to disrupt the mating behavior of insect pests that communicate by means of substrate-borne vibrations. This research falls within the new field of biotremology and it brought the VMD from a theoretical concept to practical open field experimentation: in 2017, VMD was applied in an organic vineyard in Northern Italy to control leafhopper pests’ population density. This achievement gave us the opportunity to report the state of the field for the method, to discuss the ongoing research and to make a comparison between pheromone mating disruption (PMD) and VMD. In this chapter, we review the salient moments that led to the field application of VMD. Then, we discuss the VMD characteristics and we provide a benchmark, using as reference the traditional PMD to discuss similarities and differences. Furthermore, we analyze the advantages and disadvantages of applying VMD to commercial crops. We are convinced that the first vibrational vineyard is a starting point and that biotremology will provide many innovative possibilities for farmers to control pests in the future. We also think that the introduction of electronic devices in the vineyard could be a trailblazer for the diffusion of smart technology in viticulture, thus improving its general management.

The green leafhopper, Empoasca vitis, is a polyphagous pest of grapevine and tea plants. To date population density is controlled primarily by insecticides and there is a demand for more sustainable controls. To develop a vibrational mating disruption method, the natural occurrence of a 'disruptive signal' was investigated. Further, the efficacy of natural and artificial 'disruptive signals' was determined.With behavioral trials we described male rivalry and recorded a species-specific disruptive signal (DP). The DP, a single pulse overlapping the competitor male call, interfered with the rival's ability to locate the female. Laboratory playback disruption trials revealed that the pair formation process was prevented by artificial disturbance noises that included the following features: E. vitis DP, Scaphoideus titanus disturbance noise, and a pure tone (250 Hz). Among these, the pure tone was most efficient at preventing mating.Results support development of a vibrational mating disruption method as a control strategy for E. vitis. To simultaneously disrupt the mating of E. vitis and S. titanus, the possibility of applying the S. titanus disturbance noise combined with the pure tone is discussed. © 2018 Society of Chemical Industry.

Communication through vibrational signals is widespread among social insects and regulates crucial social activities. Females of the social wasp

The mirid bugs Macrolophus pygmaeus and M. costalis use substrate-borne vibrational signals during pair formation and in male-male interactions as determined by laser vibrometry. The vibrational communication of Macrolophus is more complex than in other mirids, with a signal repertoire composed of two elements, only produced by males, while the females are mute. The 'yelp' signal consists of one or several consecutive brief pulses with harmonic structure and is commonly produced by stationary males before mating, as a key-element of courtship. 'Yelping' is also associated with contacts between males. The 'roar' signal differs from 'yelps' in that it has a broadband frequency pattern, a longer and more variable duration than 'yelping', and is produced by males in association with walking on the leaf. Playback experiments did not affect male vibration emission, but when 'roaring' was used as stimulus, it elicited a significant increase in the time spent walking. We detected significant differences between M. costalis and M. pygmaeus in some spectral parameters of the 'roar' and 'yelp' signals, so these signals could contain species-specific information. We conclude that 'roaring' and 'yelping' vibrational signals are used by Macrolophus in social communication, in particular in the context of mating behavior. CG was funded by an Erasmus Training Grant. OA was funded by the Spanish Ministry of Economy and Competitiveness (MINECO) (Project AGL2011-24349)