Impact of folivory on photosynthesis is greater than the sum of its holes

Abstract

The effects of herbivores on plant production and fitness may not relate directly to the quantity of biomass removed because folivory may alter photosynthetic rates at a considerable distance from the damaged tissue [ ]. An impediment to understanding the effects of leaf damage on photosynthesis has been an inability to map photosynthetic function within a single leaf. We developed an instrument for imaging chlorophyll fluorescence and used it to map the effects of caterpillar feeding on whole-leaf photosynthesis in wild parsnip. The adverse effects of caterpillar feeding on photosynthesis were found to extend well beyond the areas of the leaflet in which caterpillars removed tissue. These ''indirectly'' affected areas remained impaired for at least 3 days after the caterpillars were removed and were six times as large as the area directly damaged by the caterpillars. Although photosynthesis in indirectly affected areas was reduced and not eliminated, these areas accounted for three times as much of the overall reduction in photosynthesis as the area removed by the caterpillars. The size of the indirect effects was positively correlated with defense-related synthesis of furanocoumarins, suggesting that costs of chemical defense may be one factor that accounts for the indirect effects of herbivory on plants.I n average years, net primary productivity removed by herbivores ranges from 2 to 15% in forests and from 4 to 24% in oldfields and grasslands (1). However, impacts on individual plants and plant communities are not readily predicted by the amounts of tissue taken by herbivores. Such unpredictability results from a variety of phenomena, including distribution of the damage within a plant (concentrated in one area or dispersed; ref.2), specific location (e.g., proximity to a vein; ref.3), induced production of allelochemicals that can be costly to produce (4), and the potential for compensatory increases of photosynthetic rates in intact leaf tissue (5).Many of the phenomena that mediate the effects of damage on photosynthesis have been undetectable to researchers because measurement of small areas of leaves by conventional gas exchange methods has been technically impossible. We developed an instrument that spatially maps chlorophyll fluorescence of intact leaves and extends the capabilities of previous instruments by providing a complete fluorescence-quenching analysis (6), imaging of larger areas of leaves (4-6 cm 2 ), and simultaneous gas-exchange measurements. In this study, we produced high-resolution images of the quantum efficiency of photosystem II (FЈ q ͞FЈ m ). The pixel values are directly related to the rate of electron transfer through the photosystems (7) and are highly correlated with the rate of carbon dioxide assimilation (8). We used this instrument to examine the effects of caterpillar damage in wild parsnip (Pastinaca sativa), a weedy species of European origin that occurs widely in the northeastern United States. When foliage of this species is damaged, furanocoumarins, compounds with bio...

Birds defend trees from herbivores in a Neotropical forest canopy

“…For example, our estimates did not account for leaves that were abscised after arthropod damage, which could underestimate leaf loss by up to 50% (29). Also, recent work has shown that simply measuring holes in leaves, as in this study, may underestimate by a factor of 6 the actual damage to photosynthetic tissue caused by chewing insects (30).…”

Alteration of plant primary metabolism in response to insect herbivory

“…Reduced photosynthetic capacity can exceed what would be expected from the observed amount of foliar tissue that is removed (Zangerl et al, 2002). However, actual insect damage is not a prerequisite for reduced photosynthetic activity.…”

Induced defence in lima bean plants exposed to the volatiles from two-spotted spider mite-infested conspecifics is independent of the major protein expression

“…Giri et al (2006) reported that the amount of proteins involved in photosynthesis decreased in N. attenuata leaves when they were wounded and treated with oral secretions of M. sexta, which probably resulted in a reduced rate of photosynthesis. Such negative impacts from herbivory on photosynthetic activity have been reported (Zangerl et al 2002). In contrast, little change in photosynthetic activity in the volatile exposed lima bean plants was detected in a previous study (Arimura et al 2000a).…”