Vibrational playbacks and microscopy to study the signalling behaviour and female physiology of Philaenusspumarius

Abstract

The meadow spittlebug Philaenus spumarius, vector of the bacterium Xylella fastidiosa, relies on vibrational communication to accomplish mating: the female calls to establish a duet with a male. A deeper knowledge of the species’ reproductive biology and behaviour would provide useful information for developing control techniques based on principles of ‘biotremology’, which studies the vibrational behaviour of animals. Playback tests were conducted on single females and male–female pairs of P. spumarius from June to October 2018, and the features of the recorded calling signals were analysed using a wavelet decomposition. Dissections were performed on females to evaluate the relationship between calling activity and ovarioles development. From August onwards, females started to emit calling signals and to develop ovarioles. Female calling activity, duration of their chirps and their responsiveness to mating increased as the season progressed, and they were correlated with ovarioles’ development and presence of mature eggs. Hence, the ovarian maturation represents a key factor in association with the development of the sexual behaviour of P. spumarius females. Conversely, males produced advertisement signals soon after adult eclosion in May, but these signals were not involved in the pair formation process. Mating was achieved only when males produced courtship signals in response to female calling signals and established with them vibrational duets starting from August. Here, we provide new information regarding the P. spumarius’ ethology and hypothesize that potential mating disruption techniques should consider the insect physiology and be applied when both sexes are responsive to mating signals.

Intrasexual Vibrational Behavior of Philaenus spumarius in Semi-Field Conditions

“…On the other hand, although the male courtship is usually emitted by males in response to female calling signals [ 23 ], it was produced by males in the absence of females during our trials. The same behavior was also observed in absence of other males and in response to playbacks of male signals [ 24 ]. It is possible that the male calling signal triggered other males to produce courtship signals, due to similarities with the female calling (i.e., they are both composed of chirps).…”

“…This study investigated intrasexual communication and associated types of vibrational signals occurring in non-social insect groups. Under semi-field conditions (e.g., natural daylight and temperatures), the signaling behavior of P. spumarius females was recorded from the 24th of July 2018, earlier than a previous study in laboratory conditions that reported the occurrence of female mating signals from August, in correspondence with the maturation of their reproductive apparatus [ 24 ]. Females produced intersexual vibrational signals, when tested alone, in the presence of another male or when subjected to a playback only when they were sexually mature.…”

“…To evaluate the insect signaling throughout the season, trials covered most of the insect adult stage, which was divided into two parts: “early” season (from 14 June to 31 July 2018), and “late” season (from 1 August to 28 September 2018). Early and late seasons corresponded to the periods associated with the absence and presence of ovarioles in females, respectively [ 24 ]. The signaling during nighttime was not evaluated, given that pilot recordings suggested that P. spumarius has a negligeable signaling activity during night (data not shown).…”

“…The mating behavior of P. spumarius is mediated by vibrational signals and the role of intraspecific vibrational signals has already been described [ 23 ]. Since the calling behavior of females depends on their sexual maturation [ 24 ], their responsiveness to mating signals is delayed and increases through the season. Adults of P. spumarius can occur at high densities at the same and on nearby host plants [ 20 , 25 , 26 , 27 , 28 ], suggesting that their vibrational environment includes multiple individuals simultaneously signaling.…”

Xylella fastidiosa in Olive: A Review of Control Attempts and Current Management

“…Regarding the manipulation of sexual behavior, interesting investigations are ongoing to characterize the emission of vibrational signals by males and females. The first detailed description of the vibrational signals with specific roles within the mating behavior of P. spumarius was reported by Avosani et al [ 101 ]. The authors concluded that even if further research is needed to identify an efficient signal and the most suitable strategy for field application, these preliminary results open up the possibility to manipulate P. spumarius behavior through artificial playbacks and for the future development of low environmental impact control practices, for example by attracting males into a trap using a specific vibrational signal.…”