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Mexican Bean Beetle (Coleoptera: Coccinellidae) Injury Affects Photosynthesis of Glycine Max and Phaseolus Vulgaris

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Mexican Bean Beetle (Coleoptera: Coccinellidae) Injury Affects Photosynthesis of Glycine Max and Phaseolus Vulgaris PHYSIOLOGICAL AND CHEMICAL ECOLOGY Mexican Bean Beetle (Coleoptera: Coccinellidae) Injury Affects Photosynthesis of Glycine max and Phaseolus vulgaris ROBERT K. D. PETERSON,' LEON G. HIGLEY, FIKRU J. HAILE, AND JOSE A. F. BARRIGOSSI Department of Entomology, University of Nebraska-Lincoln, Lincoln, NE 68583-0816 Environ. Entomol. 27(2): 373-381 (1998) ABSTRACT Based on previous photosynthesis studies, adult Mexican bean beetles, Epilachna varivestis Mulsant, produce a different physiological response to injury in soybean than other insect defoliators. In 1993 and 1994, we conducted experiments to determine the nature and extent of photosynthetic rate reductions in soybean, Glycine max (L.) Merrill, and dry bean, Phaseolus vulgaris L. We used a randomized complete block design for all experiments. In most experiments, treatments were an uncaged, uninjured leaflet; a caged, uninjured leaflet; and a caged, injured leaflet. Treat- ments were replicated >5 times. Experimental units were individual trifoliolate leaflets. Four to 8 larvae or adults were placed in each leaflet cage and allowed to feed for 6-18 h. After feeding, the insects and leaf cages were removed and gas exchange properties were determined. Both adults and larvae reduced photosynthetic rates of the remaining tissue of the injured leaflet on both soybean and dry bean. A significant linear relationship between photosynthetic rate and percentage injury was observed for both adult and larval injury. Injury reduced photosynthetic rates in an 6 soybean and dry bean cultivars used in the experiments. There was no recovery of photosynthetic rates after injury of an individual leaflet. Stomatal conductance rates were not consistently different between injured and uninjured leaflets. Intercellular CO2 concentrations were similar or higher in injured leaflets. Consequently, reductions in photosynthesis do not seem to be attributable to stomatal limitations. Quantum efficiency was not affected by injury, indicating that light-harvesting structures were not peJ1urbed. Therefore, our results suggest that the limitations to photosynthesis are attributable to the utilization of CO2 or the supply or utilization of phosphate. Our findings suggest that the limitation is associated with RuBPcase, RuBP regeneration, or phosphate utilization. KEY WORDS Epilachna varivestis, herbivory, defoliation, gas exchange, soybean, dlY bean REsEARCHON BIOTIC stress and its effect on plant phys- ing redlegged grasshoppers, Mela.noplusfemurrubrum iology is still in its infancy. Few researchers have (DeGeer); soybean loopers, Pseudoplusia includens attempted to synthesize responses of plants to biotic (Walker); velvetbean caterpillars, Antica.rsia gemma- stresses (Welter 1989, Higley et al. 1993, Peterson and ta.lis (Hubner); green c!overworms, Pla.thypena sca.bra Higley 1993). The paucity of research on physiological (F.); soybean leafminer adults, Odontota. homi Smith; responses to biotic stress is especially apparent in the bean leaf beetle adults, Ceratoma. trifurca.ta. (Forster); area of arthropod-induced plant stress, even though and Mexican bean beetle adults, Epilachna vanvestis insect and mite injury represents one of the most Mulsant (L.G.H., unpublished data). Photosynthetic impOltant types of biotic stress (Higley et al. 1993). rates of the remaining leaflet tissue were not affected Injury by arthropods potentially can affect popula- by herbivore injury, except for the injury by Mexican tion dynamics and life history strategies of both her- bean beetles. Mexican bean beetle injury significantly bivores and plants. Characterizing the influence of reduced photosynthetic rates of the remaining leaf- arthropods on plant gas exchange processes, such as lets. However, the research discussed above and pre- photosynthesis, water vapor transfer, and respiration vious studies on soybean and several other plant spe- is important because these processes are crucial de- cies have demonstrated that both simulated and actual terminants of plant growth, yield, and fitness. There- insect defoliation do not perturb photosynthetic rates fore, characterizing physiological responses to herbi- of remaining tissue of individual, injured leaves (Wel- vores can "provide a common basis for understanding ter 1989, 1991; Higley 1992; Peterson et a1. 1992; Peter- how plants respond to insect-induced stress" (Peter- son and Higley 1993). son and Higley 1993). Injury by adult and larval Mexican bean beetles is During field research in 1989 and 1990, individual physically different from injury by other lepidopteran leaflets of soybean, Glycine max (L.) Merrill, were and coleopteran soybean defoliators. Adults and lar- exposed to injury by several insect herbivores, inc!ud- vae scrape, crush, and then consume leaf tissue, leav- ing both large and small leaf veins unconsumed, but I Dow AgroSciences, 306/2C, 9330 Zionsville Road, Indianapolis, often injured. Visually, the injured leaflet is "laced" or IN 46268. "skeletonized" (Edwards et a!. 1994). Based on pre- 0046-225X/98/0373-0381$02.00/0 © 1998 Entomological Society of America 374 ENVIRONMENTAL ENTOMOLOGY Vol. 27, no. 2 liminary photosynthesis studies, it was evident that to arthropod injury types. We addressed the following adult Mexican bean beetles also produce a different 7 questions: (1) Is larval injury similar to adult injury physiological response to injury in soybean than do in its effect on photosynthesis? (2) Does injury reduce other insect defoliators. photosynthesis in another host species, dry bean, Substantial progress has been made in determining Phaseolus vulgaris L.? (3) Does injury reduce photo- the physiological mechanisms responsible for reduc- synthesis in different soybean and dry bean cultivars? tions in photosynthetic activity. Sharkey (1985) iden- (4) Does injury reduce photosynthesis at different tified 3 categories for all limitations to photosynthe- stages of soybean and dry bean development? (5) Do sis-the supply or utilization of CO2, the supply or injured leaflets compensate for injury over time? (6) utilization of light, and the supply or utilization of Is the entire leaflet affected by injury? and (7) What phosphate. It is now possible to determine the phys- are the physiological and biochemical mechanisms iological and biochemical limitations of photosynthe- responsible for the reductions in photosynthesis? sis to environmental conditions with both in vitro and in vivo techniques. Using ecophysiological instrumen- Materials and Methods tation and biochemically based models (Farquhar and von Caemmerer 1982, Farquhar and Sharkey 1982, Indeterminate soybean was planted in 1993 ('Ken- Sharkey 1985), researchers have determined the role wood') and 1994 ('Clark 3W' and 'Clark 5N') at field of stomatal and nonstomatallimitations to photosyn- sites on the East Campus of the University of Ne- thesis in several plant systems (e.g., Sharkey and See- braska, Lincoln. The soil is a Zook silty clay loam (fine, mann 1989, Bowden et al. 1990, Pennypacker et al. montmorillonitic, mesic Cumulic Haploaquoll). All 1990, Ni and Pallardy 1992, Kicheva et al. 1994, Koch sites were disked before planting. Row orientation was et al. 1994). north-south. Row width was 76 cm and planting den- Specific biochemical limitations, such as ribulose sity was 25 plants per row-meter. (Table 1 contains 1,5-bisphosphate carboxylase/ oxygenase (RuBPcase) specific information on cultivars, treatment replica- activity, ribulose 1, 5-bisphosphate (RuBP) regener- tions, and blocking factors.) ation, and triose phosphate utilization can be deter- For the greenhouse experiments, soybean (Ken- mined fOf C3 species using a combination of assimi- wood and 'Resnick) and dry bean ('Beryl' and 'Flint') lation-intercellular CO2 response curves, quantum were planted in plastic pots (16 cm diameter) con- efficiency determinations, fluorescence measure- taining 2/3 silt loam soil and 113 sand. Each plant was ments, and metabolite assays (Sharkey 1985). Only the grown individually in a pot under a high-pressure metabolite assay is a destructive technique. Single sodium lamp (400 W), with a photoperiod of 14:10 photosynthesis measurements provide limited infor- (L:D) h. mation concerning biochemical limitations to photo- We used 9 experiments in both field and greenhouse synthesis. Therefore, assimilation-C02 response environments to address our research questions (Ta- curves and quantum efficiency determinations re- ble 1). We used a randomized complete block design quire multiple photosynthesis measurements in rela- for all experiments. In most experiments, treatments tion to changing CO2 concentrations and light inten- were an uncaged, uninjured leaflet; a caged, uninjured sities, respectively (Sharkey 1985). Unfortunately, leaflet; and a caged, injured leaflet. Treatments were much of the work on photosynthetic responses to replicated at least 5 times. Experimental units were insect injury is based on single measurements, and individual trifoliolate leaflets. Because photosynthetic studies describing gas exchange mechanisms are lack- rates vary considerably among leaves, all 3 leaflets per ing (Peterson and Higley 1993). leaf typically were used as experimental units to re- Many studies have characterized photosynthetic duce natural variability. Previous research (compari- limitations during drought stress. However, a few re- sons of caged leaflets with uncaged leaflets within a searchers have examined photosynthetic limitations to leaf, or with uncaged leaves of different plants)
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