Population biology and epidemiology of plant virus epidemics: from tripartite to tritrophic interactions

Abstract

Natural enemies have long been used in biological control programs to mitigate the damage caused by herbivory. Many herbivorous insect species also act as plant virus vectors, enabling virus transmission from plant to plant and hence disease development in a plant population. Whilst an intuitive assumption would be to expect a decrease in vector numbers to lead to subsequent reductions in virus transmission, recent evidence suggests that introduction of natural enemies (parasitoids and predators) may in some cases increase plant virus transmission while at the same time reducing vector numbers. In this paper we review the evidence for plant-virusvector-natural enemy interactions, the signalling mechanisms involved and their implications for virus transmission, and show how a modelling approach can assist in identifying the key parameters and relationships involved in determining the disease outcome. A mathematical model linking the population dynamics of a vector-parasitoid system with virus transmission was used to investigate the effects of virus inoculation and acquisition rates, parasitoid attack rate and vector aggregation on disease dynamics across a wide range of parameter value combinations. Virus spread was found to increase with enhanced inoculation, acquisition and parasitoid attack rate but decrease with high levels of vector aggregation.

Conditional Vector Preference Aids the Spread of Plant Pathogens: Results From a Model

“…For example, vector aggregation could be inßuenced by vector host preference that along with altered host volatiles from infected plants may change rates of pathogen attack (Jeger et al 2012 and references therein). Species that consume vectors may also affect the spread of plant disease (Jeger et al 2012).…”

“…For example, vector aggregation could be inßuenced by vector host preference that along with altered host volatiles from infected plants may change rates of pathogen attack (Jeger et al 2012 and references therein). Species that consume vectors may also affect the spread of plant disease (Jeger et al 2012). Indeed, predators and parasitoids have often been used to control vectors (Radcliffe and Ragsdale 2002), but they may also promote vector movement and, consequently, pathogen spread (Hodge and Powell 2008).…”

Spatio-Temporal Dynamics of Viruses are Differentially Affected by Parasitoids Depending on the Mode of Transmission

“…Furthermore, damaged plants emit the “cry-for-help” signal that may indirectly benefit hosts under herbivore attack [21]. Therefore, it is evident that there is a need to integrate all these multitrophic reactions between agents resulting in epidemiological consequences [20,21]. …”

“…Furthermore, certain species of aphids employ the ‘drop and move’ escape behaviour when they feel disturbed by foliar-foraging enemies [18,19], potentially increasing the risk of vector dispersal. Alarm pheromones play a crucial role in aphid dispersion and there have even been several attempts to mathematically model plant-virus-vector-natural enemy interactions by integrating this alarm signal, enhancing virus spread due to the presence of aphid parasitoids [20,21]. …”

Tri‐trophic interactions mediate the spread of a vector‐borne plant pathogen

“…Increased vector movement due to predators can promote pathogen spread, even though predators reduce vector abundance, by increasing the rate at which vectors encounter new hosts (Jeger et al. ). However, greater vector movement due to predators may decrease pathogen spread if moving vectors spend less time feeding (Long and Finke ).…”