Since 2013, Xylella fastidiosa Wells et al. has been reported to infect several hosts and to be present in different areas of Europe. The main damage has been inflicted on the olive orchards of southern Apulia (Italy), where a severe disease associated with X. fastidiosa subspecies pauca strain De Donno has led to the death of millions of trees. This dramatic and continuously evolving situation has led to European and national (Italian and Spanish) measures being implemented to reduce the spread of the pathogen and the associated olive quick decline syndrome (OQDS). Research has been also carried out to find solutions to better and directly fight the bacterium and its main insect vector, Philaenus spumarius L. In the course of this frantic effort, several treatments based on chemical or biological substances have been tested, in addition to plant breeding techniques and integrated pest management approaches. This review aims to summarize the attempts made so far and describe the prospects for better management of this serious threat, which poses alarming questions for the future of olive cultivation in the Mediterranean basin and beyond.

Diseases associated with Xylella fastidiosa have been described mostly in North and South America. However, during the last five years, widespread X. fastidiosa infections have been reported in a constrained area of the Apulia region (southern Italy), in olives trees suffering a severe disease, denoted as Olive Quick Decline Syndrome (OQDS). Because many xylem sap-feeding insects can function as vectors for the transmission of this exotic pathogen in EU, several research programs are ongoing to assess the role of candidate vectors in the spread of the infections. Initial investigations identified Philaenus spumarius (L.) as the predominant vector species in the olive orchards affected by the OQDS. Additional experiments have been carried out during 2016 and 2017 to assess the role of other species. More specifically, adults of the spittlebugs Philaenus italosignus Drosopolous and Remane, Neophilaenus campestris (Fallen) and of the planthopper Latilica tunetana (Matsumura) (Issidae) have been tested in transmission experiments to assess their ability to acquire the bacterium from infected olives and to infect different susceptible hosts (olives, almond, myrtle –leaf milkwort, periwinkle). Acquisition rates determined by testing individual insects in quantitative PCR assays, ranging from 5.6% in N. campestris to 22.2% in P. italosignus, whereas no acquisition was recorded for L. tunetana. Successful transmissions were detected in the recipient plants exposed to P. italosignus and N. campestris, whereas no trasmissions occurred with L. tunetana. The known vector Philaenus spumarius has been included in all the experiments for validation. The systematic surveys conducted in 2016 and 2017 provided further evidence on the population dynamics and seasonal abundance of the spittlebug populations in the olive groves.

Spittlebugs are the vectors of the bacterium Xylella fastidiosa Wells in Europe, the causal agent of olive dieback epidemic in Apulia, Italy. Selection and distribution of different spittlebug species on host-plants were investigated during field surveys in 2016–2018 in four olive orchards of Apulia and Liguria Regions of Italy. The nymphal population in the herbaceous cover was estimated using quadrat samplings. Adults were collected by sweeping net on three different vegetational components: herbaceous cover, olive canopy, and wild woody plants. Three species of spittlebugs were collected: Philaenus spumarius L., Neophilaenus campestris (Fallén), and Aphrophora alni (L.) (Hemiptera: Aphrophoridae). Philaenus spumarius was the predominant species both in Apulia and Liguria olive groves. Nymphal stages are highly polyphagous, selecting preferentially Asteraceae Fabaceae plant families, in particular some genera, e.g., Picris, Crepis, Sonchus, Bellis, Cichorium, and Medicago. Host-plant preference of nymphs varies according to the Region and through time and nymphal instar. In the monitored sites, adults peak on olive trees earlier in Apulia (i.e., during inflorescence emergence) than in Liguria (i.e., during flowering and beginning of fruit development). Principal alternative woody hosts are Quercus spp. and Pistacia spp. Knowledge concerning plant selection and ecological traits of spittlebugs in different Mediterranean olive production areas is needed to design effective and precise control strategies against X. fastidiosa vectors in olive groves, such as ground cover modifications to reduce populations of spittlebug vectors.

Philaenus spumarius L. has been identified as the main vector of Xylella fastidiosa, the bacterium causing a disease denoted as Olive Quick Decline Syndrome (OQDS) in Southern Italy. OQDS epidemics have been decimating olive orchards since 2013 and marks the first establishment and spread of this pathogen in the European territory. A major impediment to contain OQDS spread has been the lack of registered and approved pesticides for the control of P. spumarius on olive. From late 2017 to early 2018, only two commercial formulations of acetamiprid and delthametrin were officially registered in Italy. Hence, an urgent need exists to evaluate field efficacy of chemicals with different active ingredients, formulations, and modes of action to control the meadow spittlebug.

Spatial-temporal dynamics of spittlebug populations, together with transmission biology, are of major importance to outline the disease epidemiology of Xylella fastidiosa subsp. pauca in Apulian olive groves. The spread rate of X. fastidiosa is mainly influenced by (i) the pathogen colonization of the host plant; (ii) the acquisition of the pathogen by the vector from an infected plant, and its inoculation to healthy plants; (iii) the vector population dynamics and abundance at different spatial scales; and (iv) the dispersal of the vector. In this contribution we summarize the recent advances in research on insect vectors’ traits—points ii, iii, and iv—focusing on those most relevant to X. fastidiosa epidemic in Apulia. Among the vectors’ bioecological traits influencing the X. fastidiosa epidemic in olive trees, we emphasize the following: natural infectivity and transmission efficiency, phenological timing of both nymphal and adult stage, the role of seminatural vegetation as a vector reservoir in the agroecosystem and landscape, and preferential and directional dispersal capabilities. Despite the research on X. fastidiosa vectors carried out in Europe in the last decade, key uncertainties on insect vectors remain, hampering a thorough understanding of pathogen epidemiology and the development of effective and targeted management strategies. Our goal is to provide a structured and contextualized review of knowledge on X. fastidiosa vectors’ key traits in the Apulian epidemic, highlighting information gaps and stimulating novel research pathways on X. fastidiosa pathosystems in Europe. [ ] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .