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Wheat Stem Sawfly, Cephus Cinctus Norton PLANTÐINSECT INTERACTIONS Wheat Stem Sawfly, Cephus cinctus Norton, Impact on Wheat Primary Metabolism: An Ecophysiological Approach 1 TULIO B. MACEDO, ROBERT K. D. PETERSON, DAVID K. WEAVER, AND WENDELL L. MORRILL Department of Entomology, 333 Leon Johnson Hall, Montana State University, Bozeman, MT 59717Ð3020 Environ. Entomol. 34(3): 719Ð726 (2005) ABSTRACT The impact of wheat stem sawßy, Cephus cinctus Norton (Hymenoptera: Cephidae), on the photosynthetic capacity and primary metabolism of wheat, Triticum aestivum L., was evaluated in three different environments: environmental growth chamber, greenhouse, and Þeld. C. cinctus elicited different photosynthetic responses in different environments. Wheat gas exchange param- eters, such as photosynthesis, stomatal conductance, intercellular CO2, and transpiration in the growth chamber environment were negatively affected by C. cinctus feeding. Conversely, the same gas exchange responses were not observed under greenhouse and Þeld conditions. This study shows the important role of environmental variables, such as ambient CO2 concentrations and light intensity, on plant responses to herbivores. KEY WORDS Triticum aestivum, herbivory, photosynthesis, eco-physiology, injury guilds INJURY BY MANY HERBIVOROUS arthropod species has long (as traditionally had been done). Furthermore, Peter- been known to have a negative impact on plant pho- son and Higley (2001) argued that similarities in plant tosynthesis and yield in both agricultural and natural response to speciÞc injury types (also known as injury systems (Welter 1989, Peterson and Higley 1993, guilds) can be used effectively to address many basic Delaney and Macedo 2001, Peterson 2001). Charac- and applied research questions. terizing primary metabolic mechanisms, such as gas The most complete studies of arthropod injury and exchange, underlying plant responses to arthropod plant gas exchange responses involve the leaf-mass injury is needed to adequately explain Þtness and yield consumption (defoliation) injury guild (Peterson loss and develop general models of plant response 2001, Peterson et al. 2004). Other injury guilds, such as (Peterson 2001, Peterson and Higley 2001). Plant gas assimilate sapping, mesophyll feeding, and leaf mining, exchange processes, such as photosynthesis, water- have been studied much less. Virtually nothing is vapor transfer, and respiration, represent a subset of a known about plant physiological responses to the plantÕs primary metabolic processes. Consequently, stem-boring injury guild. understanding how arthropod injury inßuences these Heichel and Turner (1973) and Madden (1977) parameters is important because these are the primary suggested that stem boring impaired photosynthetic processes determining plant growth, development, capacity primarily because of injury to vascular tissue. and, ultimately, Þtness (Peterson and Higley 1993). Godfrey et al. (1991) observed reductions in photo- Furthermore, these processes respond very rapidly to synthesis of corn injured by European corn borer, external factors, so their measurement provides an Ostrinia nubilalis (Hu¨ bner). In particular, they noted immediate indication of plant stress (Peterson and 10Ð20% photosynthetic rate reductions associated Higley 1996, Peterson et al. 1998, Macedo et al. 2003). with larval stem boring and concluded that the re- Unfortunately, the physiological mechanisms un- ductions may have been related to alterations of derlying plant responses to arthropod injury are still source-sink relationships. Rubia et al. (1996) observed poorly understood (Peterson and Higley 1993, 2001). compensatory mechanisms leading to an increase in Progress in understanding plant physiological re- photosynthesis of borer-injured rice tillers. sponses to arthropod injury resulted primarily from a Plant primary metabolic responses to the wheat consideration of injury types. Boote (1981), Pedigo et stem sawßy, Cephus cinctus Norton, a larval stem al. (1986), and Higley et al. (1993) emphasized the use borer, have not been examined. C. cinctus is consid- of categorizing plant biotic stressors based on injury ered the most important insect pest of dryland wheat type and response rather than on the taxonomic clas- in the northern Great Plains. In Montana alone, losses siÞcation of stressors or physical appearance of injury by C. cinctus are approximately U.S. $25 million per year. To date, most of the research surrounding C. cinctus is 1 Corresponding author, e-mail: [email protected]. directed at aspects of detection and management. 0046-225X/05/0719Ð0726$04.00/0 ᭧ 2005 Entomological Society of America 720 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 3 However, understanding photosynthetic responses of replicates. The treatment design consisted of two wheat to C. cinctus also is of considerable practical and treatments: noninfested wheat (control) and C. cinc- theoretical interest. tusÐinfested wheat (infested). Experimental units In Montana, C. cinctus adults emerge from late May consisted of individual pots, each containing four to late June, but emergence may continue until the wheat plants. The plants and C. cinctus were main- third week of July (Criddle 1915, 1923, Wallace and tained in environmental growth chambers (Conviron) McNeal 1966, Weiss et al. 1990, Weiss and Morrill 1992, at 21 Ϯ 1ЊC, photoperiod of 14:10 (L:D) h, with a light Morrill and Kushnak 1996), which is synchronized intensity of 63 ␮mol photons/m2/s at plant level and with host plant developmental stage that is suitable for 40Ð50% RH for the duration of the study. Supplemen- C. cinctus oviposition (developmental stage 32Ð69) tal light consisted of ßuorescent lamps installed at a 3 (Zadoks et al. 1974). Generally, the uppermost inter- Cool White:1 Gro-Lux ratio (F96T12/CW/1500, nodes of an elongating stem are preferred for ovipo- F72T12/CW/1500, F96T12/GRO/VHO, and F72T12/ sition (Holmes and Peterson 1960). Each female typ- GRO/VHO; Sylvania Lighting Center, Dancers, MA). ically lays only one egg per stem (Ainslie 1920), but Gas exchange parameters, such as photosynthesis egg laying by more than one female per stem is com- (Photo), transpiration (E), and stomatal conductance mon. (gs) rates were recorded from one leaf, ßag-leaf, on Larval development may include four or Þve instars each plant using a portable photosynthesis system (Ainslie 1920), and at the onset of plant maturation, (model LI-6400; Licor, Lincoln, NE) at 1,200 ␮mol 2 ␮ larvae chew a notch around the inside perimeter of the photons/m /s light intensity, 400 mol/mol CO2 con- stem near the soil level. Infested stems usually lodge, centration, and a constant ßow of 500 ␮mol/s. A and the broken stems are highly visible to farmers smaller subset of leaves (i.e., four leaves/treatment) during harvest (Ainslie 1920). Neonate larvae initially was used to determine CO2 response curve (A-Ci) and feed on parenchyma tissue near the oviposition site light response curve. A-Ci response curves were per- (Holmes 1954). Developing larvae disperse through- formed at constant light intensity (1,500 ␮mol pho- 2 out the stems, and stem nodes are injured during the tons/m /s) and varying the intercellular CO2 (Ci) movement. Disruption of vascular tissues that are con- concentration at 50, 100, 200, 300, 400, 600, 800, and stricted at the nodes can result in an accumulation of 1,000 ␮mol/mol. material that appears as darkened areas below nodes Light-response curves or photosynthetic photon (Morrill et al. 1992b). Stems are Þlled with “frass,” ßux density (PPFD) response curves were performed consisting of fecal material and chewed plant tissue. at constant intercellular CO2 (Ci) concentration (400 ␮ ␮ Estimation of the reduction of grain resulting from mol/mol CO2) and constant ßow (500 mol/s) and larval feeding is complicated because ovipositing fe- varying light intensity at 2,000, 1,500, 1,000, 500, 200, males prefer the largest stems that have the potential 100, 50, 20, and 0 ␮mol photons/m2/s. Plant gas ex- to produce comparatively more grain (Morrill et al. change parameters were measured weekly, 17, 24, 31, 1992a). However, estimates of loss range up to 25% 38, and 45 d after removal of the plants from the cages. (Morrill et al. 1992a). Responses of A to PPFD and responses of assimilation The objective of this study was to characterize the (A) to internal CO2 concentration (Ci) were analyzed impact of injury by the stem borer, C. cinctus, on for each treatment by nonlinear regression (Layne primary metabolism of wheat. To do this, we con- and Flore 1995). The best-Þt curve was evaluated by 2 ⌫ ducted studies during 2002, 2003, and 2004 in three analysis of r . The CO2 compensation point ( ) was different environment settings: growth chamber, extrapolated as the Ci at which assimilation was greenhouse, and Þeld. 0.0 ␮mol/m2/s. Estimated carboxylation efÞciency (k) was calculated as the slope in the linear portion of the A-C response curve. Ribulose-1,5-bisphosphate Materials and Methods i (RuBP2) regeneration rate limitations were expressed Study 1. In 2002 (4 June to 19 July), we conducted by a reduced assimilation at saturating CO2 concen- a growth chamber experiment at the Plant Growth trations (Farquhar and Sharkey 1982). Carboxylation Center, Montana State University-Bozeman. Spring efÞciencies from assimilation versus Ci were deter- wheat, ÔMcNealÕ, was grown in 10.15-cm pots in a mined through linear regression analysis. Homogene- mixture of Sunshine soil mix and sand mix (1:1 ratio) ity of the independent regression
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