Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings

Arthropods and pathogens damage leaves in natural ecosystems and may reduce photosynthesis at some distance away from directly injured tissue. We quantified the indirect effects of naturally occurring biotic damage on leaf-level photosystem II operating efficiency (Phi(PSII)) of 11 understory hardwood tree species using chlorophyll fluorescence and thermal imaging. Maps of fluorescence parameters and leaf temperature were stacked for each leaf and analyzed using a multivariate method adapted from the field of quantitative remote sensing. Two tree species, Quercus velutina and Cercis canadensis, grew in plots exposed to ambient and elevated atmospheric CO2 and were infected with Phyllosticta fungus, providing a limited opportunity to examine the potential interaction of this element of global change and biotic damage on photosynthesis. Areas surrounding damage had depressed Phi(PSII) and increased down-regulation of PSII, and there was no evidence of compensation in the remaining tissue. The depression of Phi(PSII) caused by fungal infections and galls extended > 2.5 times further from the visible damage and was similar to 40% more depressed than chewing damage. Areas of depressed Phi(PSII) around fungal infections on oaks growing in elevated CO2 were more than 5 times larger than those grown in ambient conditions, suggesting that this element of global change may influence the indirect effects of biotic damage on photosynthesis. For a single Q. velutina sapling, the area of reduced Phi(PSII) was equal to the total area directly damaged by insects and fungi. Thus, estimates based only on the direct effect of biotic agents may greatly underestimate their actual impact on photosynthesis.