Global interest on plant-microbe-insect interactions is rapidly growing, revealing the multiple ways in which microorganisms mediate plant-herbivore interactions. Phytopathogens regularly alter whole repertoires of plant phenotypic traits, and bring about shifts in key chemical or morphological characteristics of plant hosts. Pathogens can also cause cascading effects on higher trophic levels, and eventually shape entire plant-associated arthropod communities. We tested the hypothesis that a Candidatus Phytoplasma causing cassava witches’ broom (CWB) on cassava (Manihot esculenta Grantz) is altering species composition of invasive herbivores and their associated parasitic hymenopterans. We conducted observational studies in cassava fields in eastern Cambodia to assess the effect of CWB infection on abundance of specialist and generalist mealybugs (Homoptera: Pseudococcidae), and associated primary and hyper-parasitoid species. CWB infection positively affects overall mealybug abundance and species richness at a plant- and field-level, and disproportionately favors a generalist mealybug over a specialist feeder. CWB phytoplasma infection led to increased parasitoid richness and diversity, with richness of ‘comparative’ specialist taxa being the most significantly affected. Parasitism rate did not differ among infected and uninfected plants, and mealybug host suppression was not impacted. CWB phytoplasma modifies host plant quality for sap-feeding homopterans, differentially affects success rates of two invasive species, and generates niche opportunities for higher trophic orders. By doing so, a Candidatus phytoplasma affects broader food web structure and functioning, and assumes the role of an ecosystem engineer. Our work unveils key facets of phytoplasma ecology, and sheds light upon complex multi-trophic interactions mediated by an emerging phytopathogen. These findings have further implications for invasion ecology and management.

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Published in PLOS ONE, v. 12, 8, e0182766, p. 1-18.

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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This initiative was conducted as part of a STINT project funded by the Swedish University of Agricultural Sciences (SLU), with additional support through a region-wide, EU-IFAD grant executed by the International Center for Tropical Agriculture CIAT (CIAT-EGC-60-1000004285). Further financial support was provided through the global, CGIAR-wide Research Program (CRP) on Roots, Tubers and Banana (RTB).

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A minimal underlying data-set has been made publicly available as Supporting Information files within a stable, public data repository, with the following URL: http://dx.doi.org/10.7910/DVN/OERIEZ.

journal.pone.0182766.s001.xlsx (19 kB)
S1 Table. Original supporting dataset for the manuscript.