Modelling interference between vectors of non-persistently transmitted plant viruses to identify effective control strategies

Abstract

Aphids are the primary vector of plant viruses. Transient aphids, which probe several plants per day, are considered to be the principal vectors of non-persistently transmitted (NPT) viruses. However, resident aphids, which can complete their life cycle on a single host and are affected by agronomic practices, can transmit NPT viruses as well. Moreover, they can interfere both directly and indirectly with transient aphids, eventually shaping plant disease dynamics. By mean of an epidemiological model, originally accounting for ecological principles and agronomic practices, we explore the consequences of fertilization and irrigation, pesticide deployment and roguing of infected plants on the spread of viral diseases in crops. Our results indicate that the spread of NPT viruses can be i) both reduced or increased by fertilization and irrigation, depending on whether the interference is direct or indirect; ii) counter-intuitively increased by pesticide application and iii) reduced by roguing infected plants. We show that a better understanding of vectors’ interactions would enhance our understanding of disease transmission, supporting the development of disease management strategies.

A climate-driven compartmental model for fungal diseases in fruit orchards: The impacts of climate change on a brown rot-peach system

“…In our model, the key variable determining the host status is the size of the fruit which increases over the season in a sigmoidal way. Incorporating epidemiology into a plant/host growth model, explicitly considering the effects of climate and agricultural practices, to assess crop yield/losses is a pivotal challenge for plant science (Cunniffe et al, 2015a;Donatelli et al, 2017;Zaffaroni et al, 2020Zaffaroni et al, , 2021. The 25 study of the response of epidemiological systems, described via compartmental SIR or SEI-like models, to a varying (in time) environment has been already done for humans (Casagrandi et al, 2006;Rinaldo et al, 2012), animal (Bolzoni et al, 2008;Samuel et al, 2011) and plant (Truscott and Gilligan, 2003) diseases.…”

Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission

“…This is most particularly the case for non-persistently transmitted viruses, although past modelling work has also targeted other transmission classes [ 68 ]. Including these complexities would be an interesting extension for our future work, particularly by linking our treatment of vector preference with other recent work addressing competition between populations of vectors which colonise a particular host population vs. those that only pause briefly on the host population as part of larger-scale migratory behaviour [ 69 ]. This would also allow us to begin to address the effects of cooperation–or otherwise–in managing vector densities for epidemics spreading within a community of growers [ 70 ].…”

Can biological control be a strategy to control vector-borne plant viruses?

“…Its effect on virus spread depends on the proportion of lost vectors (by death or emigration) replaced by immigrants and the proportion of viruliferous vectors in the immigration pool (Madden et al 2000). In systems with a continuous flow of migrants from external sources, the rate of virus spread is very high regardless of the mode of transmission because new plant infections will result both from infected plants inside the field and from vectors carrying the virus from outside the field (Roy et al 2021;Zaffaroni et al 2021). At relatively low vector immigration rate, virus incidence can reach disease saturation, which hinders the effect of natural enemies.…”

“…By contrast, non-persistently and semi-persistently transmitted virus spread are less influenced by the proportion of viruliferous immigrants because of the short times needed for acquisition and inoculation (Madden et al 2000). In their epidemiological model, Zaffaroni et al (2021) showed that even with a small proportion of viruliferous immigrants, the spread of non-persistently transmitted viruses can be continuous in the crop. When immigrants are a continuous source of vectors, we can hypothesize that management strategies to reduce the proportion of viruliferous immigrants closest to 0% reduce persistently transmitted virus primary spread within a field but will probably have less effects on non-persistently and semi-persistently transmitted virus spread.…”

“…For instance, reducing vector feeding period on host plant can limit persistently transmitted virus spread within a field (Grilli and Holt 2000). Several theoretical studies have shown that management strategies aiming at altering vector movement, by reducing the number of plants visited, are more effective in controlling plant viruses than strategies targeting vector abundances, in particular with non-persistently transmitted viruses Zaffaroni et al 2021).…”