Investigating Barley Yellow Dwarf Virus epidemiology and insecticide resistance in the English grain aphid Sitobion avenae in post-neonicotinoid Ireland

The English grain aphid Sitobion avenae is a major agricultural pest in Europe. It damages crops by transmitting barley yellow dwarf virus resulting in yield losses of up to 80%. In recent years, aphid control has become more challenging due to the emergence of resistance to pyrethroids in S. avenae. Additionally, the 2018 EU-ban on neonicotinoid seed treatments for outdoor use leaves pyrethroid as the remaining chemical control option. Therefore, it has been hypothesised that BYDV pressure in Irish winter barley will rise, due to the selection of insecticide resistant S. avenae after insecticide spray applications. Given their enormous potential agricultural impact, this research thesis first investigates whether the incidence of insecticide resistant aphids in Irish winter barley has risen, following the neonicotinoid ban. The results of a three-year field study indicated that both resistance and BYDV levels highly vary between sampling years, and that there was no evidence for linking an increased incidence of resistance in S. avenae to an overuse of pyrethroids. Additionally, the application of an insecticide was associated with an overall reduction in aphid numbers in the field. There was no evidence of the emergence of homozygous resistant clones found. However, caution is required, to prevent the emergence of new resistances in the future. Continued aphid monitoring will be a cornerstone of ensuring that changes in insecticide resistance levels or mechanisms are captured early. This thesis analysed S. avenae migration patterns and investigated the influence of weather conditions. Additionally, it aimed to assess whether resistance and BYDV levels in migrating S. avenae increased following the neonicotinoid ban. The results showed that, although S. avenae migration correlated with weather factors, there was a high variation in aphid numbers, resistance and BYDV levels depending on the sampling year and location. There was no evidence that migrating S. avenae showed increasing resistance levels throughout the three years. The ability of insecticide resistant S. avenae to transmit BYDV efficiently onto winter barley plants was investigated, following anecdotal evidence that resistant aphids could be responsible for local BYDV outbreaks. For this, transmission efficacy was investigated using two BYDV species found in Irish barley (BYDV-PAS and BYDV-MAV), and resistant and susceptible S. avenae clones. The results showed that the overall BYDV-PAS transmission rates were low for all S .avenae clones. Also, there was no significant difference in BYDV-MAV transmission rates between resistant and susceptible S. avenae. Furthermore, preliminary evidence indicated reduced virus transmission efficiency onto BYDV-tolerant winter barley plants, which could have an impact on BYDV management in the future.
The ability of BYDV to manipulate the behaviour of its aphid vector, to enhance its own spread (virus-vector manipulation theory) was investigated. The results showed that virus-carrying aphids showed a significantly enhanced dispersion, velocity and initial movement time, in comparison to virus-free aphids. Additionally, behavioural manipulation in BYDV-PAS carrying aphids was significantly stronger than in BYDV-MAV carrying aphids, which may be a compensation mechanism by the poorly transmitted BYDV-PAS to enhance its own spread. In conclusion, aphid monitoring on a local and landscape level, BYDV transmission experiments, and vector manipulation experiments showed that the importance of the insecticide resistant S. avenae for BYDV spread in Ireland is no greater than the spread by susceptible S. avenae. Furthermore, the results highlighted the complexity of the tripartite interactions between aphids, viruses, and plants, which all impact BYDV epidemiology and should be taken into consideration when developing next generation of decision support tools for Ireland and abroad.