Background: Aphids can affect cotton photosynthesis with consequent effects on yield and productivity. However, the extent to which aphid feeding affects photosynthesis and other leaf gas parameters is not well known, especially under Australian conditions. Limited studies in other countries have reported either no or negative effects on photosynthesis, however the mechanisms underlying this response are unclear. This study aimed to establish the effects of aphids on cotton photosynthesis and to quantify the relationship between aphid population density and photosynthesis. It also attempted to explain the mechanisms of some of the effects found by examining aphid stylet damage to leaf tissue and by quantifying plant wound responses that might block phloem elements and hence cause possible feedback effects from leaf sugar build-up. Finally, the secondary effects of honeydew production from aphid infestation on cotton photosynthesis were considered. Honeydew is excreted by aphids as a by-product of feeding. Its build-up on cotton leaves may block stomata and thereby reduce photosynthesis. In the field, sooty mould fungi and dust particles adhering to the sticky leaf surface could additionally reduce photosynthesis through radiation limiting effects.
Major findings: The feeding of aphids on cotton plants reduced leaf photosynthesis in two out of six experiments. In large scale field experiments increasing aphid density progressively and negatively affected gas exchange parameters with a maximum reduction in photosynthesis of 27% at a density of 27.6 aphids/cm2. A 10% decline in photosynthesis occurred at 12.9 aphids/cm2. Reduced stomatal conductance occurred sooner than photosynthetic decline at 7.7 aphids/cm2 for a 10% reduction. Aphid infested leaves were found to have a higher proportion of closed stomata than non-infested leaves. At lower aphid densities the response was inconsistent and photosynthesis was not affected, possibly due to insufficient damage levels, lower rates of callose formation and/or plant compensation. Responses of cultivars with different leaf shapes to aphid infestation were similar.
In stocking density experiments, photosynthesis and stomatal conductance declined within 8 days of infestation with initially 0.7 and 1.5 aphids/cm2. Measurements were taken repeatedly on the same infested leaves, which established a lower aphid threshold (< 4 aphids/cm2) at which stomatal conductance and photosynthesis were first affected. The relationships between gas parameters and aphid density were described by negative linear functions and no delays or increases in photosynthesis were detected at low aphid densities. Leaf temperature increased significantly during that period. Leaves did not recover after aphid removal and stomatal conductance remained lower and leaf temperature higher than the controls, indicating that leaf damage by aphids was sufficiently severe and/or that leaf age may have influenced recovery.
Light microscopy confirmed intercellular stylet pathways into phloem but was limited in assessing cellular puncture damage. Callose formation in the interveinal areas of aphid infested leaves was evidence of a plant response to damage and older leaves contained more callose due to longer exposure to aphid feeding. Increases in aphid populations corresponded to significant reductions in photosynthesis but not to simultaneous increases in leaf sugar levels of infested leaves. Hence, callose blockage of sieve elements and feedback effects due to leaf sugar accumulation did not occur. Requirement of assimilate for boll maturation, leaf age and senescence may have had overriding effects in these experiments. Callose was also found in stomatal guard cells, most likely in response to stylet punctures, though recent literature suggests it may also have a function in the control of stomatal aperture. Closure of stomata due to callose mechanisms could reduce leaf photosynthesis, however, this was not investigated as part of this work.
The effect of natural honeydew was measured in the field and was found to significantly reduce photosynthesis of leaves and stomatal conductance by 41%, however, the effect disappeared soon after honeydew was washed off. To assess the effect of honeydew without the confounding effect of aphid feeding, artificial honeydew was composed and was applied to leaves in several layers in the field and glasshouse. Photosynthesis and stomatal conductance were reduced by 18% and were affected by the coverage and thickness of the applied honeydew. Leaves did not always recover when artificial honeydew was washed off, indicating that it may have been washed off incompletely or that honeydew may have been lodged in the sub-stomatal cavity. Application of dust to honeydew further reduced photosynthesis by blocking PAR from reaching the leaf surface. Application of honeydew to the lower leaf surface reduced photosynthesis to a greater degree than its application to the upper leaf surface, implicating stomatal blockage.
This study has shown that aphid feeding reduced photosynthesis through (i) damage to leaves, resulting in stomatal closure and hence reduced conductance, and (ii) the contamination of leaf surfaces with honeydew which both impedes stomatal conductance but also accumulates dust which further reduced photosynthesis by impairing the light reaching the leaf surface.