Insecticidal Effect of Entomopathogenic Nematodes and the Cell-Free Supernatant from Their Symbiotic Bacteria against Philaenus spumarius (Hemiptera: Aphrophoridae) Nymphs

SIMPLE SUMMARY: The 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. ABSTRACT: 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.