Indirect suppression of photosynthesis on individual leaves by arthropod herbivory

Abstract

This review briefly examines the indirect effects of herbivory on photosynthesis, measured by gas exchange or chlorophyll fluorescence, and identifies four mechanisms contributing to the indirect suppression of photosynthesis in remaining leaf tissues: severed vasculature, altered sink demand, defence-induced autotoxicity, and defence-induced down-regulation of photosynthesis. We review the chlorophyll fluorescence and thermal imaging techniques used to gather layers of spatial data and discuss methods for compiling these layers to achieve greater insight into mechanisms contributing to the indirect suppression of photosynthesis. We also elaborate on a few herbivore-induced gene-regulating mechanisms which modulate photosynthesis and discuss the difficult nature of measuring spatial heterogeneity when combining fluorescence imaging and gas exchange technology. Although few studies have characterized herbivore-induced indirect effects on photosynthesis at the leaf level, an emerging literature suggests that the loss of photosynthetic capacity following herbivory may be greater than direct loss of photosynthetic tissues. Depending on the damage guild, ignoring the indirect suppression of photosynthesis by arthropods and other organisms may lead to an underestimate of their physiological and ecological impacts.

Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species

“…With this technique, it is possible to evaluate the impact of insect feeding on light reactions of plants, specifically on photosystem II (PSII) and I (PSI). Chlorophyll fluorescence techniques have been increasingly used to provide additional information on the efficiency of photochemistry, non-photochemical energy dissipation and overall photosynthetic performance (Nabity et al 2009). Such paired measurements yield information on the extent to which PSII is using the absorbed energy and the degree to which PSII is being damaged by excess light.…”

“…Such paired measurements yield information on the extent to which PSII is using the absorbed energy and the degree to which PSII is being damaged by excess light. The use of chlorophyll fluorescence imaging for rapidly detecting indirect perturbations in leaf metabolism before any effects on growth and development have been detected has increased in recent years (Aldea et al 2006;Tang et al 2006;Delaney 2008;Nabity et al 2009). So far, remarkably little is known about the effects of scale insects on the photosynthetic pigment content and on photosynthesis parameters (Vranjic 1997;Retuerto et al 2004).…”

Salix lapponum L. vs. phytophagous insects – an assessment of the risks and the reaction of plants

“…(Łabanowski & Soika, 2003). The magnitude of the insect herbivory effect on photosynthetic capacity is multifaceted, depending mostly on the type of feeding habits and the specificity of plant defense responses (Nabity et al, 2009). It has been found that plant genotypes that are capable to maintain photosynthesis under insect attack often exhibit greater resistance, which supports the hypothesis that insect-induced changes in photosynthesis are genetically programmed (Kerchev et al, 2012).…”

“…These responses affect the life processes such as photosynthesis. Among the indirect effects on physiological processes, photosynthesis disruption can have the most significant influence on plant growth and performance (Nabity et al, 2009). Moreover, several studies have revealed inhibition of photosynthesis following insect oviposition, even where eggs are laid on the leaf surface in the absence of tissue damage, which suggests that down-regulation of photosynthesis is a plant-driven response to the perception of stress rather than a secondary physiological response to tissue damage (Kerchev et al, 2012).…”

“…It is well established that the emission of chlorophyll a fluorescence provides an indicator of the primary photochemistry of photosynthesis (Murchie & Lawson, 2013). Measurements of chlorophyll a have been applied to demonstrate that impairment of the photochemistry (direct or indirect) upon insect attack is a common physiological disorder (Nabity et al, 2009;Golan et al, 2015).…”