The unique color pattern polymorphism and the foamy nymphal case of the meadow spittlebug Philaenus spumarius have attracted the attention of scientists for centuries. Nevertheless, since this species has never been considered a major threat to agriculture, biological, ecological and ethological data are missing and rather scattered. To date this knowledge has become of paramount importance, in view of the discovery of P. spumarius main role in the transmission of the bacterium Xylella fastidiosa in Italy, and possibly in other European countries. The aim of this review is to provide a state of the art about this species, with particular focus on those elements that could help developing environmental friendly and sustainable control programs to prevent transmission of X. fastidiosa. Moreover, recent findings on the role of the meadow spittlebug as vector of the fastidious bacterium within the first reported European bacterium outbreak in Apulia (South Italy) will be discussed.

Discovery of Xylella fastidiosa from olive trees with "Olive quick decline syndrome" in October 2013 on the west coast of the Salento Peninsula prompted an immediate search for insect vectors of the bacterium. The dominant xylem-fluid feeding hemipteran collected in olive orchards during a 3-mo survey was the meadow spittlebug, Philaenus spumarius (L.) (Hemiptera: Aphrophoridae). Adult P. spumarius, collected in November 2013 from ground vegetation in X. fastidiosa-infected olive orchards, were 67% (40 out of 60) positive for X. fastidiosa by polymerase chain reaction (PCR) assays. Euscelis lineolatus Brullé were also collected but tested negative for the pathogen. Transmission tests with P. spumarius collected from the Salento area were, therefore, conducted. After a 96-h inoculation access period with 8 to 10 insects per plant and a 30-d incubation period, PCR results showed P. spumarius transmitted X. fastidiosa to two of five periwinkle plants but not to the seven olive plants. Sequences of PCR products from infected periwinkle were identical with those from X. fastidiosa-infected field trees. These data showed P. spumarius as a vector of X. fastidiosa strain infecting olives trees in the Salento Peninsula, Italy.

The recent introduction of Xylella fastidiosa in Europe and its involvement in the Olive Quick Decline Syndrome (OQDS) in Apulia (Salento, Lecce district, South Italy) led us to investigate the biology and transmission ability of the meadow spittlebug, Philaenus spumarius, which was recently demonstrated to transmit X. fastidiosa to periwinkle plants. Four xylem-sap-feeding insect species were found within and bordering olive orchards across Salento during a survey carried out from October 2013 to December 2014: P. spumarius was the most abundant species on non-olive vegetation in olive orchards as well as on olive foliage and was the only species that consistently tested positive for the presence of X. fastidiosa using real-time PCR. P. spumarius, whose nymphs develop within spittle on weeds during the spring, are likely to move from weeds beneath olive trees to olive canopy during the dry period (May to October 2014). The first X. fastidiosa-infective P. spumarius were collected in May from olive canopy: all the individuals previously collected on weeds tested negative for the bacterium. Experiments demonstrated that P. spumarius transmitted X. fastidiosa from infected to uninfected olive plants. Moreover, P. spumarius acquired X. fastidiosa from several host plant species in the field, with the highest acquisition rate from olive, polygala and acacia. Scanning electron microscopy (SEM) revealed bacterial cells resembling X. fastidiosa in the foreguts of adult P. spumarius. The data presented here are essential to plan an effective IPM strategy and limit further spread of the fastidious bacterium.

First and second authors equally contributed to the work. AbstractThe recent establishment of Xylella fastidiosa subspecies pauca in the southern Italian region of Apulia threatens agricultural crops and the environment. Olive is an important and widespread ancient crop in Italy and, so far, the most impacted host. The meadow spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae) has been identified as a vector of X. fastidiosa in southern Italy; this species is one of the most common potential vectors in Europe. To generate disease management strategies, data on X. fastidiosa transmission by P. spumarius are necessary. Therefore, we carried out transmission experiments by using field-collected spittlebugs in 2014 and 2015 (5 and 11 collection dates, respectively), and transferring groups of insects immediately on to recipient plants. Various host plant species were tested: olive, oleander, sweet orange, grapevine and the stone fruit rootstock GF677 (Prunus persica 9 Prunus amygdalus). Xylella fastidiosa was detected in all the host plants after insect plant access except for grapevine; infections to sweet orange and stone fruit were not systemic. In 2015, estimates of insect X. fastidiosa infectivity were obtained; the number of PCR-positive P. spumarius on each plant was positively correlated with the plant infection status. The proportion of P. spumarius infected with X. fastidiosa ranged from 25% to 71% during the entire survey period. The number of X. fastidiosa cells detected in P. spumarius heads ranged from 3.5 9 10 to 4.0 9 10 2 (CFU equivalents), which is lower than that reported for leafhopper vectors in the Americas. These data show that field-collected P. spumarius have high rates of X. fastidiosa infection and are competent vectors.

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.

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Grapevine leafroll disease is caused by grapevine leafroll-associated viruses (GLRaVs). Within this virus complex, GLRaV-3 is the predominant species in the world. Several GLRaVs have been shown to be transmitted from vine to vine by mealybugs although a detailed characterization of transmission biology is lacking. The introduction of the vine mealybug (Planococcus ficus) in California and other regions of the world may result in increasing disease incidence of established GLRaVs. We studied the characteristics of GLRaV-3 transmission by the vine mealybug. Our results indicate that the vine mealybug transmits GLRaV-3 in a semipersistent manner. First instars were more efficient vectors than adult mealybugs. GLRaV-3 transmission lacked a latent period in the vector. Virus transmission occurred with a 1-h acquisition access period (AAP) and peaked with a 24-h AAP. Mealybugs inoculated GLRaV-3 with a 1-h inoculation access period (IAP), and transmission efficiency increased with longer plant access period up to 24 h, after which transmission rate remained constant. After an AAP of 24 h, mealybugs lost GLRaV-3 and infectivity 4 days after virus acquisition. In addition, GLRaV-3 was not transovarially transmitted from infected females to their progeny as detected by reverse transcription polymerase chain reaction. In summary, we systematically analyzed transmission parameters of GLRaV-3 by the vine mealybug and showed that transmission of this virus occurs in a semipersistent manner. This research fills in important gaps in knowledge of leafroll virus transmission, which is critical for development of leafroll disease management practices.

Spittlebugs (Hemiptera: Aphrophoridae) are the dominant xylem-sap feeders in the Mediterranean area and the only proven vectors of Xylella fastidiosa ST53, the causal agent of the olive dieback epidemic in Apulia, Italy. We have investigated the structured population phenology, abundance and seasonal movement between crops and wild plant species of both the nymphal and adult stages of different spittlebug species in olive groves. Field surveys were conducted during the 2016–2018 period in four olive orchards located in coastal and inland areas in the Apulia and Liguria regions in Italy. The nymphal population in the herbaceous cover was estimated using quadrat samplings. Adults were collected through sweep nets on three different vegetational components: herbaceous cover, olive canopy and wild woody plants. Philaenus spumarius was the most abundant species; its nymphs were collected from early March and reached a peak around mid-April, when the 4th instar was prevalent. Spittlebug adults were collected from late April until late autumn. P. spumarius adults were abundant on the herbaceous cover and olive trees in late spring, and they then dispersed to wild woody hosts during the summer and returned to the olive groves in autumn when searching for oviposition sites in the herbaceous cover. A relatively high abundance of P. spumarius was observed on olive trees during summer in the Liguria Region. The present work provides a large amount of data on the life cycle of spittlebugs within an olive agroecosystem that can be used to design effective control programmes against these vectors in infected areas and to assess the risk of the establishment and spread of X. fastidiosa to Xylella-free areas.