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Feeding behavior in relation to spittlebug transmission of Xylella fastidiosa

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Abstract

Here, we provide the first insights into the transmission dynamics of the bacterium Xylella fastidiosa by the meadow spittlebug Philaenus spumarius, gathered through DC EPG (electrical penetration graph)-assisted transmission tests and comparative observations of the probing and feeding behavior of infective versus non-infective vectors on healthy olive plants. Bacterial cells binding to P. spumarius’ foregut occurred at a very low rate and in a time as short as 15 min spent by the insect in xylem ingestion or activities interspersed with xylem ingestion (interruption during xylem ingestion and resting). P. spumarius inoculation of bacterial cells into the xylem was exclusively associated with an early (ca. 2 to 7 min after the onset of the first probe) and occasional behavior, provisionally termed waveform Xe, presumably related to egestion regulated by pre-cibarial valve fluttering. Infective spittlebugs compared to non-infective ones exhibited: (i) 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); and (iv) longer time required to perform the first probe. These observations suggest difficulties in feeding of infective P. spumarius probably caused by the presence of X. fastidiosa within the foregut. Overall, our data indicate that likely short time—few minutes—is required for X. fastidiosa transmission by P. spumarius; thus, vector control strategies should aim at preventing spittlebug access to the host plant. Furthermore, our findings represent an important contribution for further research on the disruption of spittlebug–bacterium interactions.

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Additional data will be furnished by the authors upon reasonable request.

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Acknowledgements

We are deeply thankful to Enzo Manni and Federico Manni (Coop. ACLI-Racale) for the use of the rearing and transmission facilities, and helpful discussions about sustainable containment strategies of X. fastidiosa in Salento (Apulia, South Italy). We acknowledge Francesco Palmisano, Crescenza Dongiovanni, and Giulio Fumarola (CRSFA-Basile Caramia) for plants rearing and support in field activities. We also acknowledge Giuseppe Altamura and Vincenzo Cavalieri (IPSP-CNR Bari) for technical support in laboratory analysis. An additional thank to Alexander Purcell, Adam Zeilinger, Nicola Bodino and Anna Markhaiser for helpful discussions on early experimental scheme and data analysis. This work has been financially supported by European Union Horizon 2020 research and innovation program under Grant Agreements No. 727987 XF-ACTORS (Xylella Fastidiosa Active Containment Through a multidisciplinary-Oriented Research Strategy).

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Cornara, D., Marra, M., Morente, M. et al. Feeding behavior in relation to spittlebug transmission of Xylella fastidiosa. J Pest Sci 93, 1197–1213 (2020). https://doi.org/10.1007/s10340-020-01236-4

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