Effects of Insect Herbivory on Physiological and Biochemical (Oxidative Enzyme) Responses of the Halophyte Atriplex subspicata (Chenopodiaceae)

Abstract

Physiological responses of the halophyte, Atriplex subspicata Nutt. Rydb., to defoliation injury were evaluated through a series of experiments measuring plant gas exchange, ßuorometry, and enzyme activity. Leaves exposed to simulated insect herbivory exhibited reductions in photosynthesis, stomatal conductance, and transpiration. Carboxylation efÞciency, maximum assimilation, and CO 2 compensation were also negatively associated with mechanical leaf injury. Insect injury by a herbivore generalist, Spilosoma virginica, also reduced photosynthesis and carboxylation efÞciency within the saturated spectrum of A/C i response curves. Initially, declines in photosynthesis occurred because of transient stomatal limitations. However, after time, mesophyll limitations impaired photosynthesis and the plantÕs ability to compensate for injury. Fluorescence data and light assimilation responses indicated that defoliation did not play a role in limiting light reactions of photosynthesis. Enzyme analyses showed increased peroxidase activity with insect injury, suggesting the need for future characterization of oxidative enzymes, which have been associated with traits of resistance. Overall, we found a salt-tolerant plant to be susceptible to insect herbivory through a reduction in the efÞciency of the plant to allocate energy resources. If salt tolerance comes at the cost of susceptibility to biotic interference, natural occurring halophytes or plants with transgenic salt tolerance may be at risk for heightened deleterious response to insect herbivory. KEY WORDS salt tolerance, mesophyll limitations, peroxidase, plant-insect interactions Saline wetland habitats are home to a wide array of unique ßora and fauna. Atriplex subspicata is an annual forb that occurs coastally and throughout the western United States, growing in disturbed remnant saline soil patches, alkaline ditches, and stream banks where saline seeps constantly alter the abiotic environment. Because of the paucity of data on how halophytes, including Atriplex species, respond to insect her-bivory, there is a need for understanding potential effects of herbivory on salt-tolerant plants. Saline habitats are extremely stressful environments to the organisms inhabiting them. Halophytes have built-in mechanisms that give them an advantage over nonhalophytes in saline environments. The genus Atriplex contains a wide variety of salt-tolerant species with varying saline optima (6 Ð233 mM NaCl) (Flow-ers et al. 1977); the genus also includes both C 3 and C 4 photosynthetic pathways present among differing species (Osmond et al. 1980). A number of studies have documented the effects of abiotic inßuence (e.g., temperature, salinity, photoperiod) on germination and plant zonation (Noe and Zedler 2000, 2001). Un-gar (1996) examined the response of A. patula to increased salinity across development stages and showed decreased germination, concentrated ions in tissues , and increased ash content. Atriplex patula also showed greater selenium uptake relative to 30 other Atriplex lines (Vickerman et al. 2002) and increased uptake under irrigation (Wu et al. 1993). Irrigation decreased biomass, possibly because of decreased competitive ability among neighboring glycophytes (nonsalt tolerant) or selenium toxicity (Wu et al. 1993). In examinations of halophyte photosynthesis, Atriplex species responded diversely to abiotic stress from saline conditions. In general, these studies have indicated that photosynthesis and subsequent growth are positive within the optimal salinity ranges but decrease outside these optima (Pearcy and Ustin 1984, Plaut et al. 1991, Glenn and Brown 1998). However, halophytes are subject to more than abiotic interference and must survive biotic interactions also. Few studies of Atriplex, however, have evaluated responses to biotic inßuences (e.g., herbivory, competition), and current data are limited to evaluations of competition, large scale herbivory (grazing), granivory (seed predation), and their combinations (Ungar 1998). Recent work done on foliar herbivory or arthropod injury at the leaf level by