Climate warming exacerbates plant disease through enhancing commensal interaction of co-infested insect vectors

Abstract

Pathosystems often involve two or more insect vector species; their positive or negative interactions may play key roles in plant pathogen transmission. Although climate warming likely causes changes in interactions among insect vectors by altering their demographics and behaviors, the mechanistic links between climate warming, insect vectors’ interactions, and epidemic dynamics remain largely unknown. To determine these links, we conducted a factorial experiment to determine how climate warming impacts the interactions between two coexisting insect vectors [Drosophila melanogaster (common) and Drosophila suzukii (invasive)] in relation to the development of the economically important grape sour rot disease by testing their demographic performance and pathogen transmission efficacy. To determine underlying mechanisms, we hypothesized that the wound-making behavior of D. suzukii, which breaks the skin of grapes when ovipositing (zigzag movement), is a temperature-dependent process and can be improved under warming. We found that D. suzukii promoted population growth of D. melanogaster but not vice versa, showing a commensal interaction. The co-occurrence of the two vector species accelerated pathogen transmission. Under warmer temperatures, D. suzukii made more wounds in grapes, resulting in more oviposition sites for D. melanogaster, which increased population density of D. melanogaster, and a more extensive occurrence of the plant disease. Our findings highlight a novel impact of climate warming on a pathosystem, wherein stimulation of the behavior of the invasive species facilitated the vectoring capacity of the common species, which exacerbated the occurrence of the native plant disease. This novel climate-driven process in agroecosystem provides guidance for future pest and disease prediction.

Full text

Vol.:(0123456789)
1 3
Journal of Pest Science
https://doi.org/10.1007/s10340-022-01574-5
ORIGINAL PAPER
Climate warming exacerbates plant disease throughenhancing
commensal interaction ofco‑infested insect vectors
LiangZhu1· QiXue1· GangMa1· Chun‑SenMa1,2
Received: 30 May 2022 / Revised: 29 September 2022 / Accepted: 17 October 2022
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022
Abstract
Pathosystems often involve two or more insect vector species; their positive or negative interactions may play key roles
in plant pathogen transmission. Although climate warming likely causes changes in interactions among insect vectors by
altering their demographics and behaviors, the mechanistic links between climate warming, insect vectors’ interactions, and
epidemic dynamics remain largely unknown. To determine these links, we conducted a factorial experiment to determine
how climate warming impacts the interactions between two coexisting insect vectors [Drosophila melanogaster (common)
and Drosophila suzukii (invasive)] in relation to the development of the economically important grape sour rot disease
by testing their demographic performance and pathogen transmission efficacy. To determine underlying mechanisms, we
hypothesized that the wound-making behavior of D. suzukii, which breaks the skin of grapes when ovipositing (zigzag
movement), is a temperature-dependent process and can be improved under warming. We found that D. suzukii promoted
population growth of D. melanogaster but not vice versa, showing a commensal interaction. The co-occurrence of the two
vector species accelerated pathogen transmission. Under warmer temperatures, D. suzukii made more wounds in grapes,
resulting in more oviposition sites for D. melanogaster, which increased population density of D. melanogaster, and a more
extensive occurrence of the plant disease. Our findings highlight a novel impact of climate warming on a pathosystem,
wherein stimulation of the behavior of the invasive species facilitated the vectoring capacity of the common species, which
exacerbated the occurrence of the native plant disease. This novel climate-driven process in agroecosystem provides guid-
ance for future pest and disease prediction.
Keywords Climate change· Commensalism· Pathogen transmission· Drosophila melanogaster· Drosophila suzukii·
Grape sour rot
Introduction
Ongoing climate warming can not only directly impact spe-
cies’ performance (Ma etal. 2015, 2021;Olsen etal. 2016;
Tougeron etal. 2018; Zhu etal. 2021), but also mediate their
interactions with other species and subsequently change
these species’ performance indirectly (Canto etal. 2009;
Davis etal. 1998; Gilman etal. 2010). Such indirect changes
in species’ performance can generate cascading responses,
which require corresponding changes in pest and disease
management strategies in agroecosystems (Eigenbrode etal.
2018). Agroecosystems commonly consist of crop plants,
herbivorous insects, and pathogens and other components.
Crop plants play a key role in crop production, as well as
environmental improvement (Ratnadass etal. 2012); how-
ever, cultivated plant species are commonly damaged by
phytopathogens (Strange and Scott, 2005) and herbivorous
Communicated By Nicolas Desneux.
Liang Zhu and Qi Xue have contributed equally to this work.
* Chun-Sen Ma
machunsen@caas.cn
1 Climate Change Biology Research Group, State Key
Laboratory forBiology ofPlant Diseases andInsect
Pests, Institute ofPlant Protection, Chinese Academy
ofAgricultural Sciences, No 2 Yuanmingyuan West Road,
Haidian District, Beijing100193, People’sRepublicofChina
2 School ofLife Science, Institute ofLife Science andGreen
Development, Hebei University, Baoding071002, China
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