Abstract

Simple SummaryThe disease caused by Xylella fastidiosa affects economically relevant crops such as olives, almonds, and grapevine. Since curative means are not available, its current management principally consists of broad-spectrum pesticide applications to control vectors like the meadow spittlebug Philaenus spumarius, the most important one in Europe. Exploring environmentally sound alternatives is a primary challenge for sustainable agriculture. Entomopathogenic nematodes (EPNs) are well-known biocontrol agents of soil-dwelling arthropods. Recent technological advances for field applications, including improvements in obtaining cell-free supernatants from EPN symbiotic bacteria, allow their successful implementation against aerial pests. Here, we investigated the impact of four EPN species and their cell-free supernatants on nymphs of the meadow spittlebug. First, we observed that the exposure to the foam produced by this insect does not affect the nematode virulence. Indeed, direct applications of certain EPN species reached up to 90–78% nymphal mortality rates after five days of exposure, while specific cell-free supernatants produced 64% mortality rates. Overall, we demonstrated the great potential of EPN and cell-free supernatant of their symbiont bacteria applications against this vector, opening new venues to develop novel biopesticides for integrated management practices and organic productions.The meadow spittlebug Philaenus spumarius (Hemiptera: Aphrophoridae) is the primary vector of Xylella fastidiosa (Proteobacteria: Xanthomonadaceae) in Europe, a pest–disease complex of economically relevant crops such as olives, almonds, and grapevine, managed mainly through the use of broad-spectrum pesticides. Providing environmentally sound alternatives to reduce the reliance on chemical control is a primary challenge in the control of P. spumarius and, hence, in the protection of crops against the expansion of its associated bacterial pathogen. Entomopathogenic nematodes (EPNs) are well-known biocontrol agents of soil-dwelling arthropods. Recent technological advances in field applications, including improvements in obtaining cell-free supernatant from their symbiotic bacteria, allow their successful implementation against aerial pests. Thus, this study aimed to evaluate, for the first time, the efficacy of EPN applications against nymphal instars of P. spumarius. We tested four EPN species and the cell-free supernatant of their corresponding symbiotic bacteria: Steinernema feltiae–Xenorhabdus bovienii, S. carpocapsae–X. nematophila, S. riojaense–X. kozodoii, and Heterorhabditis bacteriophora–Photorhabdus laumondii subsp. laumondii. First, we showed that 24 and 72 h exposure to the foam produced by P. spumarius nymphs did not affect S. feltiae virulence. The direct application of steinernematid EPNs provided promising results, reaching 90, 78, and 53% nymphal mortality rates after five days of exposure for S. carpocapsae, S. feltiae, and S. riojaense, respectively. Conversely, the application of the cell-free supernatant from P. laumondii resulted in nymphal mortalities of 64%, significantly higher than observed for Xenorhabdus species after five days of exposure. Overall, we demonstrated the great potential of the application of specific EPNs and cell-free supernatant of their symbiont bacteria against P. spumarius nymphs, introducing new opportunities to develop them as biopesticides for integrated management practices or organic vineyard production.

Highlights

  • The xylem-inhabiting Gram-negative bacterium Xylella fastidiosa (Proteobacteria: Xanthomonadaceae) can damage several relevant crops that affect the global farming economy.The main problem associated with these diseases is the obstruction of the xylem, with symptoms ranging from leaf marginal necrosis and leaf abscission to dieback, delayed growth, and death of plants through insufficient water flow [1,2]

  • The foam produced for nymphs of P. spumarius affected neither 7EPN

  • Since the foam could protect the applied infective juvenile (IJ) and facilitate their movement to locate the nymphs, our results suggest that the direct application of Entomopathogenic nematodes (EPNs) suspensions in the spit–nymph complex might be compatible and a promising method to control the pest in crops

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Summary

Introduction

The xylem-inhabiting Gram-negative bacterium Xylella fastidiosa (Proteobacteria: Xanthomonadaceae) can damage several relevant crops that affect the global farming economy.The main problem associated with these diseases is the obstruction of the xylem, with symptoms ranging from leaf marginal necrosis and leaf abscission to dieback, delayed growth, and death of plants through insufficient water flow [1,2]. The meadow spittlebug Philaenus spumarius (Hemiptera: Aphrophoridae) is considered the principal vector of X. fastidiosa in Europe and an emergent threat for several perennial crops, including vineyards and olive and almond groves [6,7]. This xylem sapfeeding insect has a univoltine life cycle and the eggs can diapause over winter for more than one hundred days, adults survive if the climate is appropriate [8]. A recent study completed in the Iberian Peninsula has shown that this spittlebug mainly occurs in the spring season on herbaceous ground vegetation in olive groves across Southern, Eastern, and Central Spain and Northeastern

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