Insights into the transmission dynamics of Xylella fastidiosa by Philaenus spumarius

The establishment and relentless spread of the bacterium Xylella fastidiosa in some areas in Europe call for effective containment measures based on sustainable control strategies. However, the development of such strategies requires a thorough characterisation of the reciprocal interactions among the three key factors of the pathosystem, i.e. the bacterium, the vector, and the host plant. One of the major differences between European and American or Taiwanese epidemics refers to the vector species driving bacterium spread. Indeed, while sharpshooters (Hemiptera: Cicadellidae) are the key vectors in all the X. fastidiosa outbreaks other than European ones, spittlebugs such as Philaenus spumarius seem to play the main role in bacterial spread in Europe. Currently, knowledge about X. Fastidiosa–spittlebug interactions and the characterisation of the mode of transmission considerably lags behind the background on sharpshooters. Here we began to fill this knowledge gap by carrying out EPG (Electrical Penetration Graph)-assisted transmission tests of X. fastidiosa by P. spumarius (acquisition from infected olive plants and inoculation of healthy olives and oleanders). Furthermore, we conducted comparative observations on the probing and feeding behaviour of infective versus non-infective spittlebugs on healthy olive plants. Spittlebug acquisition rate of X. fastidiosa from olive appeared to be extremely low; bacterial cells binding to the foregut occurred in a time as short as 15 minutes spent by the insect in xylem ingestion or activities interspersed with xylem ingestion (interruption during xylem ingestion and resting). Either in olive or oleander, P. spumarius inoculation of bacterial cells into the xylem was associated with an early (2.5 to 7 minutes after the onset of the first probe) and occasional behaviour, visualised by a specific DC-EPG waveform (Xe), presumably related to egestion of fluids regulated by pre-cibarial valve fluttering following a lack of phagostimulation. Behaviours stereotypically repeated by the insect and commonly performed during most of the probes did not lead to bacterial inoculation to the host plant. Infective spittlebugs compared with non-infective spittlebugs exhibited: i) significantly longer non-probing and shorter xylem ingestion; ii) longer duration of single non-probing events; iii) fewer sustained ingestions (ingestion longer than 10 min) and interruptions of xylem activity (N); iv) longer time required to perform the first absolute probe. These observations suggest difficulties in feeding for infective P. spumarius probably caused by the presence of X. fastidiosa in the foregut. Overall, our findings open new perspectives for research on the X. fastidiosa–spittlebug relationship and for sustainable control strategies based on the disruption of bacterium–vector interaction.