Published in Agron J 100:720-725 (2008)
DOI: 10.2134/agronj2007.0066
© 2008 American Society of Agronomy
677 S. Segoe Rd., Madison, WI 53711 USA
POTATO
Second Generation European Corn Borer Injury and Irish Potato Physiology, Yield, and Quality
Jesse R. Ziemsa,
W. Wyatt Hobackb,*,
Leon G. Higleyc,
Thomas E. Huntd,
Odair A. Fernandese,
Cristina Bastosf and
Adeney de Freitas Buenog
a CSS Farms, 2016 32 Rd., Minden, NE 68959
b Dep. of Biology, Univ. of Nebraska, Kearney, NE 68849
c Dep. of Entomology, Univ. of Nebraska, Lincoln, NE 68583-0816
d Dep. of Entomology, Univ. of Nebraska Haskell Agricultural Lab., 57905 866 Rd., Concord, NE 68728
e UNESP–São Paulo State Univ., Dep. de Fitossanidade Jaboticabal, SP, 14884-900, Brazil
f EMBRAPA Algodão, Primavera do Leste, MT, Brazil
g EMBRAPA SOJA, Londrina, PR, Brazil
* Corresponding author (hobackww{at}unk.edu).
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ABSTRACT
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European corn borer (ECB) [Ostrinia nubilalis (Hübner)] (Lepidoptera: Crambidae) is known to infest Irish potato (Solanum tuberosum L.) but only causes economic damage during the first generation in East Coast potato producing areas. However, in Nebraska, second generation ECB infest potato plants during the bulking period and may reduce yield and/or potato quality. Experiments were conducted in 2001, 2002, and 2003 to examine physiological and yield effects of second generation ECB injury to potato in Nebraska. Pike, Atlantic, and three Frito Lay proprietary varieties (FL1867, FL1879, and FL1833) were used. Experimental plots were infested with four ECB egg masses per plant to simulate ECB infestation by second-generation larvae; controls received no egg masses. Photosynthetic rates, tuber weights, tuber size grades, solids, and fry quality were measured. Potato plants with ECB infestation had significantly reduced photosynthetic rates on ECB-infested stems and on uninfested stems on the same plant when larvae were in the fifth instar. When insects were in the fourth instar, photosynthetic rates were reduced only on ECB-infested stems. In 2001, ECB infestation reduced the average mass of large tubers and increased the amount of small tubers in FL1867 and FL1879. In 2002, significant yield reductions were not observed. Across both years, ECB-infested plots produced fewer large (65- to 100-mm diam.) tubers than control plots. Other tuber properties and chip qualities were unaffected. This study indicates that second generation ECB infestation of approximately 30% infested plants results in economic loss for some chipping varieties and affects tuber bulking. In contrast to east coast growers, Midwest potato farmers must be concerned with second generation ECB.
Abbreviations: ECB, European corn borer
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NOTES
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All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
Received for publication February 16, 2007.
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INTRODUCTION
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EUROPEAN CORN BORER is one of the most damaging insect pests of corn (Zea mays L.) in North America. In addition to corn, ECB can also be a major pest of potato. In the north central United States, over-wintered fifth instars end diapause, pupate, and begin to emerge as adults in mid-May to early June (Mason et al., 1996). When potatoes are present and corn is in early whorl or in tasseling/silking stages, potato can be an attractive host for oviposition (Anderson et al., 1984).
In potato on the east coast, damage is generally limited to first generation ECB, while second generation ECB are not considered to cause economic damage (Kennedy, 1983; Nault and Kennedy, 1996a). In the absence of plant diseases such as black leg, bacterial soft rot (Erwinia spp.), or other abiotic factors, feeding by first generation ECB larvae on potato also does not cause detectable yield loss. Second generation ECB are not considered pests in the eastern production region because potato senescence and harvest typically occurs in June. During June, potato is less attractive for oviposition than corn, and if infested, is harvested before significant injury by second-generation larvae occurs (Kennedy and Anderson, 1983; Anderson et al., 1984). In Nebraska, however, planting dates of potato and corn are temporally similar, and potato are harvested later in the growing season. The peak flights of second generation ECB occur in early August, approximately 4 wk before commercial potato harvest in Nebraska, providing the opportunity for ECB to infest and injure potato.
First and second instars cause injury to leaves, while later instars bore in and out of potato stems creating as many as four tunnels per larva (Nault and Kennedy, 1996b). These entry wound sites typically occur in the lower third of the main stems (Kennedy and Anderson, 1983), making the plant more susceptible to wind damage and bacterial infection. For example, the bacterial disease potato blackleg, caused by Erwinia carotovora, is spread by first generation ECB as the larvae move from stem to stem (Anderson et al., 1981). However, secondary infection by this disease cannot account for all cases of economic loss attributed to ECB injury (Nault et al., 2001).
Numerous borer holes around a stem will also increase the chances that vascular tissue will be severed, stopping the flow of nutrients altogether. In addition to causing vascular injury and leaf area loss, boring injury may also result in physiological injury to the plant, however, this possibility has not been investigated. In early research it was found that potato plants with three or more borer holes per plant produced a significant amount of cull potatoes compared to plants with less than three borer holes per plant (Jones et al., 1939).
Photosynthetic output is the foundation of plant growth and yield (Peterson and Higley, 2001). While bacterial infection appears to cause the most significant problems, stem damage from ECB feeding also affects transpiration rates and leads to local wilting of leaves and eventual leaf death (Cranshaw and Radcliffe, 1980; Hare, 1980; Wellik et al., 1981; Kennedy, 1983). Although various studies have been conducted examining first generation ECB injury to potato (e.g., Hanzlik et al., 1997; Kennedy, 1983; Nault et al., 2001; Nault and Kennedy, 1996a), the physiological basis for tuber yield reduction caused by ECB injury remains unresolved.
The objectives of this study were to (i) examine if stem injury caused by second generation ECB influences the gas exchange parameters of leaves on the stem injured by the larvae and on other stems on the same plant; and (ii) examine the effects of infestation of potato by second-generation ECB on potato yield and market parameters.
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MATERIALS AND METHODS
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Experiments were conducted at two locations in commercial fields near Minden in Kearney County, Nebraska. In 2001, the experimental site was a center pivot irrigated field with Valentine loamy fine sand soil (mixed, mesic Typic Ustipsamments). In 2002 and 2003, the experimental site was a linear move pivot irrigated field with Simeon sandy loam soils (mixed, mesic Typic Ustipsamments). Planting dates were 7 May 2001, 17 May 2002, and 15 May 2003. Production practices for water, nutrient, herbicide, insecticide, and fungicide applications were consistent with those in the region.
Because experiments were conducted in production fields, different cultivars were used each year. Cultivars for 2001 were: Pike, Atlantic, FL1867, and FL1879; for 2002: Pike, Atlantic, FL1833, and FL1879; and for 2003: Pike. Varieties were located in widely distributed fields and thus, physiological measures were taken on a subset of varieties each year.
We anticipated that physiological effects of insect injury might be more severe on cultivars with determinate growth habit, so we used at least one determinate cultivar in each year and also examined some indeterminate cultivars in 2002. Of cultivars used, Atlantic characteristics include early maturity, determinate growth, tubers round to oval, and high specific gravity for tubers. The numbered varieties are Frito Lay proprietary chipping cultivars. FL1867 has determinate growth habit, early maturity, and relatively dense canopy; FL1833 has determinate growth habit, late maturity, and relatively dense canopy; and FL1879 has indeterminate growth habit, very lush canopy, continuous vegetative growth which replaces senesced leaflets, no flowering, late maturity, high yields, large tubers, and large tuber set at canopy closure. Pike is a chipping variety with mid- to main-season maturity, vigorous early vine growth, determinate growth habit, and dense canopy. All cultivars were artificially infested with European corn borer egg masses that were placed in the field on 28 July in 2001, 31 July, and 9 August in 2002, and on 20 July in 2003 to coincide with second flight and damage from second generation larvae.
The experimental design was a randomized complete block with four replications. Treatment design was a strip split plot for 2001 and 2002. The experimental design in 2003 was a randomized complete block. Experimental units were 8 rows wide by 6.1 m long. Main plots were potato cultivars, subplots were two levels of second generation ECB infestation for 2001 and 2002. Experimental ECB levels were established by simulated infestation with ECB egg masses obtained from French Agricultural Research, Inc., Lamberton, MN. Potato plants were artificially infested by pinning egg masses, when egg masses were at blackhead stage, to the undersides of leaves during the evening, usually 1 to 2 h before dark. There were two treatment levels: infested (four egg masses per plant) and check plots (no egg masses). Natural infestations of ECB were prevented by aerial application of a cyfluthrin pesticide approximately 4 d before infestations.
Potato Physiological Response
Photosynthetic rates and other gas exchange parameters of individual leaflets were measured to determine plant response to ECB injury using a portable photosynthesis system (Li-Cor Model LI 6400, Li-Cor, Lincoln, NE) equipped with a Li-6400–01 CO2 injector system. A standard 2 by 3 cm leaf chamber was used to measure a 6 cm2 area, the maximum leaf area measured by the leaf chamber. Because we took readings on days with full sun, we made measurements at 1400 µmol photons m–2 s–1 light intensity using the Li-6400–02B LED light source. Leaves were exposed to 400 µmol mol–1 CO2 concentration with a flow rate of 500 µmol per second. Assimilation-internal CO2 curves and associated parameters were determined for all treatments with four replications. Curves were determined using the automatic A-Ci program of the LI 6400. Photosynthetic parameters including respiration, vcmax, jmax, triose phosphate utilization, and stomatal limitations were calculated with the Photosynthesis Assistant version 1.2 software package (Dundee Scientific, Dundee, UK).
Stomatal conductance was also measured using the LI-6400 in 2002 and 2003. Leaflet water potential was measured in 2001 using a plant water status console (Model 3005, Soil moisture, Santa Barbara, CA) to quantify the level of moisture stress for stems on plants infested with corn borer larvae for two varieties, Pike and FL1879.
Standardized measurement of the terminal leaflet of the fourth leaf down the stem was used to ensure that leaflets were of approximately equal age. Treatments were established in a randomized block and photosynthetic rates were measured on injured stems, uninjured stems (on the same plant), and uninfested plant with no injured stem as a check. Photosynthetic measures were taken during the fifth larval stage of ECB in 2001 and 2002 and fourth larval stage in 2003. In 2003 fluorescence was also measured in the same leaves used for gas-exchange parameters. Measurements of fluorescence were taken after the leaves were dark adapted for 20 min using "adaption clips" (Li-Cor). Readings were made using a leaf chamber fluorometer (Model Licor-6400–40, Li-Cor).
Potato Yield and Quality Response
Infestation by ECB was quantified by recording stand counts and number of injured stems. Yield response was assessed by measuring plot tuber yield, tuber size parameters, solids content, and chipping quality. Size parameters for potato were graded through hexagon sizing screens into four different size categories: oversize (>102 mm), large (101–65 mm), small (64–47 mm), and undersize (<47 mm). Yield was not quantified in 2003.
Because these varieties are used to manufacture potato chips, processing parameters of specific gravity, fry quality, and external and internal defects were also measured. Specific gravity was measured by suspending potato plants in a container of water and recording the displacement by using an SFA potato hydrometer (Snack Food Association, Alexandria, VA). Fry quality was tested using standard chip frying methods and examining chip discoloration. Internal and external defects recorded were hollow heart, internal brown syndrome, vascular browning, greening, scab, bruising, rot, and attached stolons.
Statistical Analyses
Data were checked for normality and equal variance and then were analyzed using ANOVA or PROC MIXED to identify significant treatment effects (Sigma Stat 2.03 or SAS 9.1). Means were separated by protected LSD.
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RESULTS
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In all trials, pinning of egg masses to potato plants resulted in approximately 30% infestation. This relatively low rate of infestation results from mortality of early instars associated with natural enemies and irrigation effects and is similar to that observed in other studies (Sparks et al., 1967; Nault and Kennedy, 1996b). In 2001 and 2002 leaves on O. nubilalis-infested stems visually exhibited various stages of wilt and demonstrated significantly reduced photosynthetic rates on all varieties except FL1833 (Tables 1
and 2
). Rate reductions ranged from 27% (Pike, 2002) to 80% (Pike, 2001), with an average rate reduction across all varieties (except FL1833) and years of 57%. Rate differences between 2001 and 2002 may reflect differences in weather condition between years; 2001 was average while 2002 was hotter and drier than normal. In addition, readings in 2002 were taken later when potato plants were beginning to senesce.
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Table 1. Mean (SE) photosynthetic rates and stomatal conductance of potato leaflets subjected to Ostrinia nubilalis injury in 2001, 2002, and 2003. Photosynthetic rates (µββmol CO2 fixed/m2/s) were determined approximately 20 d after plants were infested when larvae were at fifth instar. In 2003, photosynthesis and fluorescence data were collected on plants infested with fourth instar O. nubilalis. Within variety, data followed by the same letter are not significantly different by protected LSD, P  0.05.
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Table 2. Mean photosynthetic parameters from analysis of assimilation-internal CO2 curves, and main effect of treatment for each parameter by ANOVA. Where a significant main effect was indicated (respiration and Vcmax), the infested treatment was significantly lower than other treatments by LSD.
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Beyond the reductions in photosynthesis associated with O. nubilalis infestation, we also observed surprising impacts of infestation on uninfested stems of infested plants in 2001 and 2002 when carbon exchange rates were taken while insects were in the fifth larval stage (Table 1). Significant reductions in photosynthesis were noted in four of six varieties examined. Across all cultivars in 2001 and 2002, uninfested stems of infested plants had approximately 50% of the photosynthetic rate reduction compared to control plants. This level of rate reduction was very close to that of infested stems (57%). In 2003, measurements were taken earlier in the season when ECB was at fourth instar, and carbon exchange rates were significantly reduced only on infested stems (Table 1).
Reductions in photosynthesis are either because of stomatal limitation in CO2 availability or mesophyll limitations. Because O. nubilalis larvae bore into the potato stem, it would be tempting to attribute photosynthetic rate reductions to disruptions in plant water relations. However, in 2001 there were no significant differences in leaf water potential among treatments (Fig. 1
). Moreover, analysis of results from A-Ci curves (Fig. 2
, Table 2) showed no evidence of significant differences in stomatal limitations between infested and uninfested plants.
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Fig. 1. Average water potential (-bars) and 1 SE of leaves on a stem infested with European corn borer, leaves on the same plant but in a stem uninfested by corn borer, and check for two varieties FL1879 and Pike in 2001.
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Fig. 2. Assimilation-internal COs curves for uninfested (control) plants; European corn borer infested plant, infested stem; and European corn borer infested plant, uninfested stem. Curves shown are averages and 1 SE from curves on plants in four replications.
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Fluorescence measurements provide an indication of function of light harvesting and photoelectron transport (Macedo et al., 2003). No difference among fluorescence readings were detected between infested plants and non-infested plants (data not shown). In support of this result, A-Ci data did not show treatment differences in jmax (PAR saturated electron transport) of in triose phosphate utilization. The ECB infested stems did have significant reductions in Vcmax, the maximum carboxylation rate by Rubisco (ribulose-1,5-bisphosphate carboxylase). Consequently, the photosynthetic reductions are associated with reduced capacity for carboxylation, rather than stomatal limitation.
Despite measuring substantial photosynthetic rate reductions in 2001 and 2002, no significant yield reductions from O. nubilalis infestation (at approximately 30% infested plants) occurred in 2001 (Table 3
). Significant total yield reductions were found in FL1879 in 2002 which had a significant infestation by variety interaction, indicating that FL1879 was more susceptible to O. nubilalis infestation than other varieties in 2002. Despite lack of significant reductions in yield, all but two infested treatments had reduced yields (Table 3). The FL1867 was unique in showing a higher yield for infested plots in 2001.
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Table 3. Main effects and interactions of varieties and second generation European corn borer (ECB) infestation (infested plots had approximately one larva per stem in 30% of plants). Also shown are means and SEs (in parentheses) of control and infested plots by variety for total yield (t/ha), and yields (t/ha) of three chipping sizes (potato diameters) for 2 yr. Significance was judged as P 0.05.
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The major bulking period (Allen and Scott, 2001), representing maximal movement of photosynthate and stored carbohydrate from leaves to tubers, occurred slightly after infestation of O. nubilalis. In 2001, two varieties, FL1879 and FL1867, had differences in size grades, showing that in circumstances of reduced photosynthate availability, plants respond by filling across tuber sizes, rather than increasing sizes of the larger tubers (Table 3). For FL1879 experimental plots had significantly higher t/ha for small tubers and significantly lower t/ha for large tuber compared to controls. Variety FL1867 also had significantly more t/ha for small tubers in experimental plots than for controls. Although not statistically significant, controls had about 5.61 t/ha more large tubers.
Although ECB infestation appeared to reduce the amount of large tubers for certain varieties, no significant differences were observed among processing parameters. Specific gravity, fry quality, external and internal defects were all similar among experimental plots and controls (data not shown).
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DISCUSSION
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Previous studies of O. nubilalis on potato have highlighted the importance of O. nubilalis infestation in contributing to blackleg infections. The bacterial disease potato blackleg is spread by first generation ECB as the larvae move from stem to stem (Anderson et al., 1981) and can result in significant economic loss (Nault et al., 2001). However, Nault et al. (2001) suggested that secondary infection by the disease cannot account for all cases of economic loss attributed to ECB injury. Here, we were able to examine the influence of O. nubilalis on primary plant metabolism and on yields independent of other stressors. Our results point to a striking impact of late instar larval O. nubilalis infestation on whole plant photosynthesis. Additionally, our data show that O. nubilalis have the potential to reduce potato yields especially by affecting size classes of tubers used in chipping; however, substantial tolerance to O. nubilalis exists. After artificial infestations, stem counts showed approximately 30% of plants to have at least one stem infested by an ECB larva. Our yield data suggest that in the absence of disease interactions, second generation ECB infestation levels as high as 30% may not significantly reduce potato yields (Table 3).
The ability of potato plants to establish plant canopies that maximize light interception early in the season is directly related to yield potential (Allen and Scott, 2001). Potato plants with a large leaf canopy may be able to tolerate high photosynthetic rate reductions if their total capacity for carbon fixation (a function of light interception and photosynthetic rates) remains above that needed for maximal yield. Previously Ziems et al. (2006) found remarkable tolerance to simulated defoliation in FL1879, an indeterminate variety of chipping potato. As in this study, size grades were affected and are economically important because small-sized tubers are less valuable for commercial chipping.
Potential to cause economic loss is also related to other stresses faced by the potato crop. Of these other stresses, disease appears to be more important than simultaneous loss of leaf area which was examined by Nault and Kennedy (1996a). Aerial soft rot follows ECB tunneling with high correlation for first generation infestation in June (Nault et al., 2001). Less than 5% soft rot and other stem diseases was observed during our trials (J. Ziems, personal communication, 2001, 2002).
Data from 2001 and 2002 demonstrate a strong reduction in photosynthesis with O. nubilalis infestation, and tentatively indicate that these reductions are associated with mesophyll limitations and not disrupted water relations. These observations imply that rate reductions associated with infestation are a systemic plant response to injury and not merely a mechanical disruption of transport tissues. The differences between varieties in photosynthetic responses of uninfested stems may imply that genetic differences exist among potato varieties in their ability to tolerate O. nubilalis injury. However, FL1879, which showed no significant reduction in uninfested stems in 2001, did show substantial (50%) photosynthetic reductions in 2002, so environmental variability rather than varietal genetics may play a more significant role in mediating tolerance to O. nubilalis infestation. In 2003, examination of photosynthetic response when larvae were in the fourth instar found reductions only on the infested stem. This observation strongly suggests that whole plant response occurs only during the last larval instar when borers are large.
Photosynthetic reductions of 50% from O. nubilalis infestation appear to have the potential to cause yield reductions in potato. However, the relationship between photosynthetic rates and yield reductions from O. nubilalis will depend on the proportion of infested plants and the photosynthetic capacity of plants, which may vary with time of infestation, differences among varieties, and different environmental conditions.
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ACKNOWLEDGMENTS
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Assistance on this project was provided by John Wallace, Benjamin Zechmann, Jeffrey Hamik, Brian Sass, and Mathew Manning. Support for A. F. Bueno was provided through a fellowship from the agreement CAPES, Brazil and Fulbright, U.S. program. Research support was provided by CSS farms, a grant from the University of Nebraska Research Services Council, and grants from the Nebraska Potato Board for supporting this project. Additionally, this project was supported by the University of Nebraska-Lincoln Agricultural Experiment Station numbers 17-068, 17-080, and 17-086. This is paper number 1280 from the Department of Entomology, University of Nebraska-Lincoln.
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
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ABSTRACT
INTRODUCTION
