Abstract

Complex multi-trophic interactions in vectorborne diseases limit our understanding and ability to predict outbreaks. Arthropod-vectored pathogens are especially problematic, with the potential for novel interspecific interactions during invasions. Variations and novelties in plant–arthropod–pathogen triumvirates present significant threats to global food security. We examined aspects of a phytoplasma pathogen of citrus across two continents. ‘Candidatus Phytoplasma aurantifolia’ causes Witches' Broom Disease of Lime (WBDL) and has devastated citrus production in the Middle East. A variant of this phytoplasma currently displays asymptomatic or ‘silent’ infections in Brazil. We first studied vector capacity and fitness impacts of the pathogen on its vectors. The potential for co-occurring weed species to act as pathogen reservoirs was analysed and key transmission periods in the year were also studied. We demonstrate that two invasive hemipteran insects—Diaphorina citri and Hishimonus phycitis—can vector the phytoplasma. Feeding on phytoplasma-infected hosts greatly increased reproduction of its invasive vector D. citri both in Oman and Brazil; suggesting that increased fitness of invasive insect vectors thereby further increases the pathogen's capacity to spread. Based on our findings, this is a robust system for studying the effects of invasions on vectorborne diseases and highlights concerns about its spread to warmer, drier regions of Brazil.

Highlights

  • Renan Batista Queiroz1, Philip Donkersley1, Fábio Nascimento Silva2, Issa Hashil Al-Mahmmoli3, Abdullah Mohammed Al-Sadi3, Claudine Márcia Carvalho2 and Simon L

  • Based on our results though, ‘Ca. Phytoplasma aurantifolia’ may not be transovarially transmitted by D. citri due to its genome size and a shorter co-evolutionary history with ‘Ca. Phytoplasma aurantifolia’, because D. citri was only reported in Oman from 2005 [31]

  • We found that the infection by ‘Ca. Phytoplasma aurantifolia’ on C. aurantifolia seedlings was lower during winter across Oman, and was higher in the Samael area in autumn, winter and summer compared with the rest of the country

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Summary

Introduction

Renan Batista Queiroz, Philip Donkersley, Fábio Nascimento Silva, Issa Hashil Al-Mahmmoli, Abdullah Mohammed Al-Sadi, Claudine Márcia Carvalho and Simon L. Complex multi-trophic interactions limit our understanding of the epidemiology of pathogens vectored by invasive insect pests and restrict our ability to predict the course of invasions. This in turn reduces our capacity to predict and manage threats to global health and food security. Persistent modes of vectorborne plantpathogen transmission, whether propagative or non-propagative (i.e. circulative), are understood to generate selection for the plant pathogen to suppress plant defences against the vector, leading to fitness benefits to both the insect vector and pathogen [12] This is true for phytoplasma and viral pathogens [11,12]. The interaction between insect vector and plant pathogen is mutualistic: the pathogen contributes to increased vector population growth on infected plants, which increases the pathogen’s capacity to disperse in new individuals of the vector [12,13]

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