The bacterium Xylella fastidiosa re-emerged as a plant pathogen of global importance in 2013 when it was first associated with an olive tree disease epidemic in Italy. The current threat to Europe and the Mediterranean basin, as well as other world regions, has increased as multiple X. fastidiosa genotypes have now been detected in Italy, France, and Spain. Although X. fastidiosa has been studied in the Americas for more than a century, there are no therapeutic solutions to suppress disease development in infected plants. Furthermore, because X. fastidiosa is an obligatory plant and insect vector colonizer, the epidemiology and dynamics of each pathosystem are distinct. They depend on the ecological interplay of plant, pathogen, and vector and on how interactions are affected by biotic and abiotic factors, including anthropogenic activities and policy decisions. Our goal with this review is to stimulate discussion and novel research by contextualizing available knowledge on X. fastidiosa and how it may be applicable to emerging diseases.

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.

There is little information available on Xylella fastidiosa transmission by spittlebugs (Hemiptera, Cercopoidea). This group of insect vectors may be of epidemiological relevance in certain diseases, so it is important to better understand the basic parameters of X. fastidiosa transmission by spittlebugs. We used grapevines as a host plant and the aphrophorid Philaenus spumarius as a vector to estimate the effect of plant access time on X. fastidiosa transmission to plants; in addition, bacterial population estimates in the heads of vectors were determined and correlated with plant infection status. Results show that transmission efficiency of X. fastidiosa by P. spumarius increased with plant access time, similarly to insect vectors in another family (Hemiptera, Cicadellidae). Furthermore, a positive correlation between pathogen populations in P. spumarius and transmission to plants was observed. Bacterial populations in insects were one to two orders of magnitude lower than those observed in leafhopper vectors, and population size peaked within 3 days of plant access period. These results suggest that P. spumarius has either a limited number of sites in the foregut that may be colonized, or that fluid dynamics in the mouthparts of these insects is different from that in leafhoppers. Altogether our results indicate that X. fastidiosa transmission by spittlebugs is similar to that by leafhoppers. In addition, the relationship between cell numbers in vectors and plant infection may have under-appreciated consequences to pathogen spread.The bacterium Xylella fastidiosa is an economically important plant pathogen that is present throughout the Americas, Europe (Italy and France), Asia (Taiwan), and the Middle-East (Almeida and Nunney 2015). The lifestyle of X. fastidiosa requires the colonization of insect and plant hosts; in addition, natural dispersal is solely mediated by insect vectors (Chatterjee et al. 2008). Therefore, knowledge about insect and plant colonization, as well as plant-to-plant transmission can guide the development of control strategies for diseases caused by X. fastidiosa. Traditionally, research has focused on how this pathogen colonizes host plants, with some but more limited attention given to insect hosts. In addition, some of the key parameters of X. fastidiosa vector transmission have been determined.Insect vectors belong to three groups of xylem sap-feeding insects, the sharpshooter leafhoppers (Hemiptera: Cicadellidae Cicadellinae), spittlebugs (Hemiptera: Cercopoidea), and cicadas (Hemiptera: Cicadoidaea). There are only two reports of cicadas as vectors (Krell et al. 2007;Paião et al. 2002), and because of the limited information more research is required on the role of these insects in X. fastidiosa spread. The first identified X. fastidiosa vectors were sharpshooter leafhoppers (Hewitt and Houston 1946;Hewitt et al. 1942). Frazier and Freitag (1946) demonstrated that several leafhopper species transmitted X. fastidiosa, information which decades later led Frazier (1965) to propose ...

Local climatic conditions are important determinants of disease dynamics through effects on vector population performance or distribution. Yet, climate may also be epidemiologically significant due to effects on host−pathogen infection dynamics. We developed a model to explore interactive effects between climate-mediated acceleration in disease phenology (i.e., faster incubation or symptom onset) and vector preference based on host symptom status. Higher incubation rates favored pathogen outbreaks, but more rapid symptom onset may constrain spread if vectors avoid symptomatic hosts. Next, we tested whether warmer conditions favored greater spread of the plant pathogen, Xylella fastidiosa, by its leafhopper vector, Graphocephala atropunctata. Inoculated and healthy plants were reared in two temperature-controlled greenhouses. At six times postinoculation, a healthy and inoculated plant were exposed to noninfective vectors, after which pathogen spread was evaluated. Incubation rate and symptom onset in infected hosts was significantly accelerated at higher temperature. Although there was a tendency for greater pathogen spread at higher temperature, the effect depended on time since inoculation. In later introductions, after disease symptoms manifest, vectors were more likely to be found on healthy hosts. Vector avoidance of symptoms, particularly for hosts reared at higher temperature, constrained pathogen spread at later introductions. These results indicate that climate and vector behavior may mediate interactively pathogen spread. Further consideration of such epidemiological complexities is needed to predict adequately the consequences of climate change for disease dynamics.

The adoption of transgenic Bt cotton has, in some cases, led to environmental and economic benefits through reduced insecticide use. However, the distribution of these benefits and associated risks among cotton growers and cotton-growing regions has been uneven due in part to outbreaks of non-target or secondary pests, thereby requiring the continued use of synthetic insecticides. In the southeastern USA, Bt cotton adoption has resulted in increased abundance of and damage from stink bug pests, Euschistus servus and Nezara viridula (Heteroptera: Pentatomidae). While the impact of increased stink bug abundance has been well-documented, the causes have remained unclear. We hypothesize that release from competition with Bt-susceptible target pests may drive stink bug outbreaks in Bt cotton. We first examined the evidence for competitive release of stink bugs through meta-analysis of previous studies. We then experimentally tested if herbivory by Bt-susceptible Helicoverpa zea increases stink bug leaving rates and deters oviposition on non-Bt cotton. Consistent with previous studies, we found differences in leaving rates only for E servus, but we found that both species strongly avoided ovipositing on H. zea-damaged plants. Considering all available evidence, competitive release of stink bug populations in Bt cotton likely contributes to outbreaks, though the relative importance of competitive release remains an open question. Ecological risk assessments of Bt crops and other transgenic insecticidal crops would benefit from greater understanding of the ecological mechanisms underlying non-target pest outbreaks and greater attention to indirect ecological effects more broadly.