Aphid herbivory decreases primary production in natural ecosystems and crop yield in agricultural systems. The mechanism for how aphids reduce yield is poorly understood as some studies suggest aphid feeding directly impedes photosynthesis, whereas other studies suggest a change in allocation of resources from growth to defense compounds reduces yield. Plants typically respond to aphid feeding with salicylic acid-dependent defenses as opposed to jasmonic acid-dependent defenses. In Nicotiana species, aphid herbivory reduces yield and transcription of photosynthetically related genes but it is unknown what defense response modulates aphid attack and if this response alters resource allocation from growth to defense. If aphid feeding reduces transcription of genes regulating photosynthesis and ultimately yield, then it is likely that herbivore damage reduces carbon sequestration. However, if photosynthesis is not reduced under aphid attack, then the reduction in yield is caused by the reallocation of resources from growth to defense. To test this hypothesis, Nicotiana attenuata plants, native tobacco, were infested with Myzus persicae, green peach aphids, at low and high densities. We quantified plant performance (growth, photosynthesis, and defense response) through time and assessed ultimate fitness (seed production). Leaf photosynthesis was measured using an open-system infrared gas analyzer and concentrations of plant defense hormones, including jasmonic acid (JA) and salicylic acid (SA), were quantified using liquid chromatography and mass spectrometry. To test the direct defense capacity of salicylic acid on aphid performance, we fed aphids an artificial diet with varying levels of SA and measured their survivorship and fecundity.
Results/Conclusions
Aphid herbivory reduced growth, final biomass, and seed set at both low and high aphid infestation levels; however, no reductions in photosynthetic gas exchange or the operating efficiency of photosystem II (i.e. the electron transport driver for carbon reduction) occurred with aphid feeding. Aphid feeding did not affect JA levels in any of the treatments, but increased SA levels under high density aphid attack during the flowering stage. Increased SA levels during the flowering stage suggest that salicylic acid accumulates over longer periods of time and its production is dependent on aphid density. Feeding trials using SA concentrations 2-3 times lower than occurred in infested flowering plants caused decreased aphid fecundity, suggesting that SA is an effective chemical defense response against aphids. The results suggest that as aphid densities increase, resources are mobilized for defense via the salicylic acid pathway, decreasing the availability of resources for growth and reducing yield.