Insect–plant–pathogen interactions as shaped by future climate: effects on biology, distribution, and implications for agriculture

Abstract

Carbon dioxide (CO 2 ) is the main anthropogenic gas which has drastically increased since the industrial revolution, and current concentrations are projected to double by the end of this century. As a consequence, elevated CO 2 is expected to alter the earths' climate, increase global temperatures and change weather patterns. This is likely to have both direct and indirect impacts on plants, insect pests, plant pathogens and their distribution, and is therefore problematic for the security of future food production. This review summarizes the latest findings and highlights current knowledge gaps regarding the influence of climate change on insect, plant and pathogen interactions with an emphasis on agriculture and food production. Direct effects of climate change, including increased CO 2 concentration, temperature, patterns of rainfall and severe weather events that impact insects (namely vectors of plant pathogens) are discussed. Elevated CO 2 and temperature, together with plant pathogen infection, can considerably change plant biochemistry and therefore plant defense responses. This can have substantial consequences on insect fecundity, feeding rates, survival, population size, and dispersal. Generally, changes in host plant quality due to elevated CO 2 (e.g., carbon to nitrogen ratios in C3 plants) negatively affect insect pests. However, compensatory feeding, increased population size and distribution have also been reported for some agricultural insect pests. This underlines the importance of additional research on more targeted, individual insect-plant scenarios at specific locations to fully understand the impact of a changing climate on insect-plant-pathogen interactions.

The promises and challenges of research on plant–insect–microbe interactions

“…As a consequence of global warming, the outcomes of plant-insect-microbe interactions are likely to be modified by future climate. Trębicki et al (2017) summarized the current knowledge on the impacts of climate change on plant, insect (both as herbivore or vector) and phytopathogen interactions. Their review brings convicing evidence that plant biochemistry and physiology are altered by increased CO 2 and temperature, with considerable consequences for defence responses against pests and pathogens.…”

“…In general, the strong impacts of endosymbionts on nutritional requirements, digestive and detoxification abilities, stress protection, and ecological niche of their insect hosts (Skidmore & Hansen, 2017;Zhang et al, 2017) have spurred interest in how to manipulate them to increase the success of beneficial insects or reduce the performance of pest insects, another big challenge in the field. Finally, with the rise of the field of microbial mediation of plantinsect interactions, novel directions continuously open up, owing to new insights in the complexity of this type of interactions, and in response to an urgent need to adapt tomorrow's agriculture to food demand and global changes (Trębicki et al, 2017). For instance, recent studies have revealed that many of the microbes that had originally been classified as entomopathogens or insect-associated microbes in fact play important roles in plants during their extensive plant endophytic stage, and vice versa, with important consequences for the plant-microbe-insect interactions.…”

Plant phenolics mediated bottom‐up effects of elevated CO2 on Acyrthosiphon pisum and its parasitoid Aphidius avenae

“…CO 2 ‘fertilization’ typically stimulates plant photosynthetic rate, increases plant growth, carbon : nitrogen (C : N) ratio and secondary metabolites in C3 plants (Ainsworth & Long, ; Lindroth, ; Dáder et al ., ; Vassiliadis et al ., ). The assimilation and reassignment of C and N resources in plants under elevated CO 2 (eCO 2 ) can alter the quality of host plants, which in turn influences the performance of herbivorous insects and even tri‐trophic natural enemies (Chen et al ., ; Stiling & Cornelissen, ; Coll & Hughes, ; Sun et al ., ; Trębicki et al ., ).…”

“…Global atmospheric CO 2 concentrations have increased from 280 µL/L before industrialization to 405 µL/L in 2017 (https://www.co2.earth/), and are predicted to reach enemies (Chen et al, 2005a;Stiling & Cornelissen, 2007;Coll & Hughes, 2008;Sun et al, 2011;Trębicki et al, 2017). eCO 2 generally increases the concentrations of phenolics in C3 plants (Peltonen et al, 2005;Matros et al, 2006), and total phenolics and flavonoids in the nitrogenfixation plants under eCO 2 increase much more than the non-nitrogen-fixation plants (Robinson et al, 2012).…”

Influence of elevated CO2 on development and food utilization of target armyworm Mythimna separata fed on transgenic Bt maize infected by nitrogen-fixing bacteria

“…The recent forecast indicated that atmospheric CO 2 concentration will increase to approximately 900 ppm by 2100 (IPCC, 2014). Increasing atmospheric CO 2 concentration alone can be very significant in crop production because of its direct effect on plant physiology and biochemistry (Cornelissen, 2011), and indirect effect on tri-trophic interactions involving plants, herbivores, and predators or pathogens (Robinson et al, 2012; Trębicki et al, 2017). Elevated atmospheric CO 2 also affects the crop production via direct or indirect impact on the physiology and feeding behavior of phytophagous insects (Zvereva & Kozlov, 2006; Massad & Dyer, 2010; O’Neill et al, 2010).…”