Abstract
Plant pathogens can profoundly affect host plant quality as perceived by their insect herbivores, with potentially far-reaching implications for the ecology and structure of insect communities. Changes in host plants may have direct effects on the life-histories of their insect herbivores, which can then influence their value as prey to their natural enemies. While there have been many studies that have explored the effects of infection when plants show symptoms of disease, little is understood about how unexpressed infection may affect interactions at higher trophic levels. We examined how systemic, asymptomatic, and seed-borne infection by the ubiquitous plant pathogen Botrytis cinerea, infecting two varieties of the lettuce Lactuca sativa, affected aphids (the green peach aphid, Myzus persicae) and two widely used biocontrol agents (the parasitoid Aphidius colemani and the ladybird predator Adalia bipunctata). Lettuce varieties differed in host plant quality. Asymptomatic infection reduced chlorophyll content and dry weight of host plants, irrespective of plant variety. Aphids reared on asymptomatic plants were smaller, had reduced off-plant survival time and were less fecund than aphids reared on uninfected plants. Parasitoids showed reduced attack rates on asymptomatically infected plants, and wasps emerging from hosts reared on such plants were smaller and showed reduced starvation resistance. When given a choice in an olfactometer, aphids preferentially chose uninfected plants of one variety (Tom Thumb) but showed no preference with the second (Little Gem) variety. Parasitoids preferentially chose aphids on uninfected plants, irrespective of host plant variety, but ladybirds did not show any such preference. These results suggest that the reduced quality of plants asymptomatically infected by Botrytis cinerea negatively affects the life history of aphids and their parasitoids, and alters the behaviors of aphids and parasitoids, but not of ladybirds. Fungal pathogens are ubiquitous in nature, and this work shows that even when host plants are yet to show symptoms, pathogens can affect interactions between insect herbivores and their natural enemies. This is likely to have important implications for the success of biological control programs.
Highlights
Plant pathogens are ubiquitous in nature, affecting the growth and development of many plant species, and reducing the quality of the plant as experienced by herbivores [1]
Asymptomatic infection by Botrytis cinerea resulted in reduced chlorophyll and plant dry weight for both plant varieties, but there was no effect on plant height (Table 2)
We demonstrate that the parasitoid A. colemani was negatively affected by asymptomatic infection, exhibiting a reduction in parasitism rate, growth rate, and starvation resistance, suggesting that the consequences of such hidden infections may ramify through trophic interactions, we do not know if this is a simple consequence of host size reduction, or some more subtle change in plant/pathogen chemistry
Summary
Plant pathogens are ubiquitous in nature, affecting the growth and development of many plant species, and reducing the quality of the plant as experienced by herbivores [1]. Most notably, chewing insects and necrotrophic pathogens (e.g., Botyrtis) can induce the jasmonic acid (JA) dependent defense pathway, while sap-sucking insects, and biotrophic pathogens, induce the salicylic acid (SA) dependent defense pathway [10] As these pathways crosstalk [11], attack by one pathogen or herbivore can induce defenses that affect another, changing perceived plant quality [12]. Both of these cues play an important role in mediating ecological interactions among plants and insects [16,17,18,19], in terms of host plant location and choice
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