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Published in Crop Sci 39:1332-1340 (1999)
© 1999 Crop Science Society of America
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Crop Science 39:1332-1340 (1999)
© 1999 Crop Science Society of America

CROP PHYSIOLOGY & METABOLISM

Maize Morphology and Shoot CO2 Assimilation after Root Damage by Western Corn Rootworm Larvae

Walter E. Riedella and R.Neil Reeseb

a USDA-ARS, Northern Grain Insects Research Lab., 2923 Medary Ave., Brookings, SD 57006 USA
b Biology-Microbiology Dep., South Dakota State Univ., Brookings, SD 57007 USA

wriedell{at}ngirl.ars.usda.gov


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 Materials and methods
 Results
 Discussion and conclusion
 REFERENCES
 
Knowledge of the physiological stress mechanisms triggered by corn rootworm larval feeding damage may suggest new ways of maintaining maize (Zea mays L.) productivity in plants damaged by this important insect pest. Western corn rootworm [Diabrotica virgifera virgifera (LeConte)] larval feeding damage to maize root systems causes complex changes in leaf CO2 assimilation. The objective of our study was to further explore the relationships between plant morphology and CO2 assimilation in rootworm-damaged maize. The effects of moderate or severe root damage caused by larval feeding or by mechanical damage on root system morphology, shoot dry weight, leaf area, stomatal conductance, and CO2 assimilation were investigated in greenhouse experiments. Rootworm larval feeding, which removed about 75% of the total root system volume, or mechanical cutting treatments imposed at the V12 leaf stage, which removed about 30% of the total root system volume, had no effect upon leaf CO2 assimilation but significantly reduced stomatal conductance when measured at the tassel development stage. During the time when larvae were damaging root systems or when specific root node axes were mechanically cut, however, leaf CO2 assimilation was less in root-damaged plants than in undamaged plants. Larval-damaged root systems had accelerated adventitious root axis growth and development in the nodes located immediately above the damaged nodes. This compensatory root growth was more pronounced under the moderate root feeding damage treatments than in the severe root damage treatments. Total leaf area and shoot CO2 assimilation were less in plants with severe larval feeding damage than in plants with moderate damage or in control plants. Thus, the severity of root damage plus the level of root compensatory growth play important roles in mediating shoot growth and CO2 assimilation responses to stress imposed by rootworm larval feeding.


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
Materials and methods
 Results
 Discussion and conclusion
 REFERENCES
 
INSECT PESTS cause severe economic losses to farmers by reducing crop yield and quality as well as increasing crop production costs (Heinrichs, 1988). Corn rootworm (Diabrotica sp.) are the most serious insect pest complex in the major maize (Zea mays L.) producing regions of the north central USA and Canada (Levine and Oloumi-Sadeghi, 1991). Western corn rootworm [Diabrotica virgifera virgifera (LeConte)] are univoltine (single generation per year) and have 3 larval developmental stages (Krysan, 1986). The soil environment, especially temperature, drives growth and development of both the rootworm larvae (Jackson and Elliott, 1988) and the maize root system (Russell and Scott, 1977). Because of the common dependence on soil environment, larval stages and root development occur in a synchronized manner under field conditions (Riedell, 1993). Rootworm larvae prefer to feed upon succulent new growth of nodal root axes. Very specific nodes of root axes, namely the 3rd through 6th, produce succulent new growth near the base of the maize plant during the time of egg hatch and larval development. This synchrony of root system and larval growth and development causes larval feeding damage to occur on specific nodes of the adventitious root system (Apple and Patel, 1963; Riedell, 1989). The resulting crop physiological stress often leads to significant grain yield loss (Sutter et al., 1990; Spike and Tollefson, 1991; Godfrey et al., 1993b; Riedell et al., 1996). Knowledge of the crop physiological stress mechanisms triggered by rootworm larval feeding damage may suggest entirely new ways of maintaining maize productivity in the presence of these insect pests (Riedell, 1993).

Interactions between corn rootworm larvae and the host plant root system take place in a subterranean arena (Branson, 1986) that is difficult to observe without its physical destruction (Buman et al., 1994; Riedell and Schumacher, 1994). Consequently, the impact of larval feeding damage on root physiology is not well documented (Welter, 1989). Field and greenhouse experiments have shown that corn rootworm damage affects shoot biomass accumulation (Spike and Tollefson, 1991), canopy temperature (Schaafsma et al., 1993), water relations (Riedell, 1990), stem sap flow (Gavloski et al., 1992), and mineral nutrient relations (Kahler et al., 1985). In general, these shoot physiological parameters were not significantly affected by slight to moderate rootworm feeding damage (one or fewer nodes of adventitious root axes destroyed), but were reduced by severe rootworm feeding damage (more than one node of root axes destroyed). Larval feeding damage effects on leaf CO2 assimilation, however, appear to be an exception to this generalization. Godfrey et al. (1993a) found that leaf CO2 assimilation measured during maximum injury (feeding by 3rd stage larvae) and postinjury (after the larval population entered the non-feeding pupal stage) were not significantly affected by moderate or severe larval feeding damage. These authors, as well as others, have concluded that CO2 assimilation measurements based on single leaf samples taken at one time point during the day are not indicative of canopy photosynthesis, and that more detailed evaluations of corn rootworm larval feeding effects on canopy photosynthesis were needed (Godfrey et al., 1993a; Hou et al., 1997). Thus, the objective of our study was to explore further the relationships between plant morphology and CO2 assimilation in maize damaged by corn rootworm larval feeding.


   Materials and methods
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and methods
Results
 Discussion and conclusion
 REFERENCES
 
Experiment Descriptions
Two experiments designed to study the relationships between root damage caused by western corn rootworm larval feeding and maize plant morphology and CO2 assimilation were conducted in greenhouses at the Northern Grain Insects Research Laboratory near Brookings, SD. Experiment 1 examined the effect of root damage caused by larval feeding or mechanical cutting on CO2 assimilation of individual leaves. Experiment 2 examined the effects of root damage effects caused by larval feeding on CO2 assimilation of entire shoots. Each experiment was repeated twice.

The two runs of Exp. 1 had different mechanical damage procedures and leaf CO2 assimilation measurement times. In Exp. 1A, approximately 25 and 75% of the entire root system was mechanically damaged and ear leaf CO2 assimilation and stomatal conductance were measured at the tassel developmental stage (VT; Ritchie et al., 1992). In Exp. 1B specific root nodes were mechanically removed and leaf CO2 assimilation measurements started at the 7th leaf stage (V7) and continued until tassel emergence.

The two runs of Exp. 2 also differed slightly from each other. In Exp. 2A, we measured shoot CO2 assimilation when the rootworm larvae reached the late 3rd stage of development, as determined by soil growing degree day accumulation (Riedell, 1989). For Exp. 2B, we measured shoot CO2 assimilation when the larvae reached the pupal development stage (Riedell, 1989).

Plant Material and Larval Infestation
For all experiments, maize kernels (A632 x A619 single cross hybrid) were planted in a 2:1:1 sandy loam soil:peat:perlite mixture contained in 46-cm diam. cellulose-fiber pots. Pots contained in 39-cm plastic saucers were placed into the greenhouse and the soil mix saturated with tap water. Six glass tubes (1.5-cm diam.) were placed vertically into the soil at a distance of about 5 cm from the kernel to facilitate larval infestation (Riedell, 1989). Soil growing degree day (GDD) accumulation (base 11°C, the lower threshold temperature for larval development; Chiang, 1973) at 15 cm below the soil surface was monitored with probes connected to biophenometers. Planting dates and greenhouse environmental conditions are shown in Table 1 . Pots were grouped into a 3- by 5-m area within the greenhouse. In Exp. 1, three high pressure sodium lamps (1000 W, General Electric, Glen Allen, VA) suspended 3 m over the pots were used to supplement natural light for the first and last 4 h of a 12-h photoperiod. In Exp. 2, six metal halide and four high pressure sodium lamps (1000 W, General Electric, Glen Allen, VA) were used to supplement natural sunlight with a 14-h photoperiod. In both experiments, a large (91-cm diam.) industrial fan, set to run coincident with the supplemental lighting, provided robust air circulation (enough to rustle the leaves of the plants) in the greenhouse. Plants were watered as needed (about once per week) by placing water in the saucer. Every third week, 10 g of Peters general purpose (20-20-20) water soluble fertilizer (J.R. Johnson, St. Paul MN) was added to each saucer before watering.


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  		Table 1 Planting dates, infestation dates, and greenhouse environmental conditions during the experiments

 
Larvae in the early 2nd stage of development (as determined by head capsule size; Branson, 1986) were obtained from the rearing colony at the Northern Grain Insects Research Laboratory and transferred into vials containing 20 g of sieved soil (80 mesh, 150 g kg-1 moisture). Glass rods were removed from the soil, and the resulting holes filled with the soil containing rootworm larvae (Riedell, 1989). Pots treated with uninfested soil served as controls. Four pots per treatment were set up in both runs of Exp. 1 while in 5 pots per treatment were used in both runs of Exp. 2. The experimental design for all experiments was a randomized complete block. Pots were infested with rootworm larvae when the plants were in the V7 leaf stage for both runs of experiment 1, the V5 to V6 stage in Exp. 2A, or the V6 stage in Exp. 2B. Rootworm larval development was monitored in both runs of Exp. 1 using additional pots treated with rootworm larvae as indicated above. Rootworm larvae were separated from root systems (Fisher, 1987) at regular time intervals after infestation. Head capsule measurements were used to determine larval development stage (Branson, 1986).

In Exp. 1A, mechanical root damage was inflicted when the majority of the rootworm larvae reached the pupal stage of development (V12 leaf stage, 505 soil GDD, 48 d after planting). Roots were cut on one side or on three sides of the plant, approximately 3 cm from the base of the stem. Vertical cuts were made to a depth of 15 cm with a sharpened spatula blade as previously described (Fitzgerald et al., 1968; Riedell, 1990).

In Exp. 1B, two mechanical root damage treatments were inflicted 7 d after larval infestation treatments started (shoots in V9 leaf stage, 419 soil GDD, 45 d after planting). For the first treatment, root axes from the 4th node, which were about 15 to 18 cm long with no lateral branching yet evident, as well as those from the 5th node, which were about 2 to 3 cm long, were severed within 0.5 cm of the stem with a scalpel. For the second treatment, only 5th node root axes were removed. At a later time during the experiment (shoots in the V10 to V11 leaf stage, 473 soil GDD, 51 d after planting) the 6th node of root axes were also removed from both mechanical cut treatments.

Leaf and Shoot Measurements
In Exp. 1A, CO2 assimilation and stomatal conductance of ear leaves were measured at the VT stage (585 soil GDD, 54 d after planting). Leaf CO2 assimilation measurements were taken in the middle of the leaf using a portable photosynthesis system (Model LI-6200; LI-COR, Inc., Lincoln, NE) fitted with a 1-L leaf chamber that sampled a leaf area of 24 cm2. Abaxial stomatal conductance was measured on the same portion of the leaf using a steady state porometer (Model LI-1600M; LI-COR, Inc.). For Exp. 1B, leaf CO2 assimilation measurements were made in the middle of the youngest leaf with a ligule (Ritchie et al., 1992) starting when the plants were at the V7 leaf stage (345 soil GDD, 37 d after planting) and ending when the plants reached the tassel development stage (589 soil GDD, 63 d after planting). For both runs of Exp. 1, measurements were made following established protocols (LI-COR, 1982, 1987) between 1100 and 1300 h on clear days with about 1000 µmol m-2 s-1 photosynthetically active radiation. No additional leaf or shoot measurements were taken in Exp. 1.

In Exp. 2, shoot CO2 assimilation measurements were performed 42 d after planting (432 soil GDD for Exp. 2A and 486 soil GDD for Exp. 2B). Plants were in the V9 leaf stage (Exp. 2A) or the V12 leaf stage (Exp. 2B) at this time. A photosynthesis measurement chamber (0.16 m3, 30 cm deep by 68 cm wide by 81 cm tall for Exp. 2A; 0.33 m3, 30 cm deep by 68 cm wide by 162 cm tall for Exp. 2B) attached to a LI-6200 portable photosynthesis system (LI-COR, Inc.) was used to measure shoot CO2 assimilation. The chambers, constructed with 0.32-cm-thick plexiglass and angle iron, contained 1 (Exp. 2A) or 2 (Exp. 2B) air circulating fans (model #4C550, Dayton Inc., Chicago, IL) that thoroughly mixed the air when the chamber was sealed. Each fan had an air movement rate of 3 m3 min-1. For both experiment runs, the entire shoot of the plant, with the exception of that portion of the stem between the soil surface and the top lip of the pot (about 4 cm), was placed in the measurement chamber. Gas exchange measurements were made between 1330 and 1500 h. Bright, hazy sky conditions plus the supplemental lighting provided 420 to 430 µmol m-2 s-1 for Exp. 2A and 450 to 470 µmol m-2 s-1 for Exp. 2B throughout the measurement period as measured by a photosynthetically active radiation sensor (model #LI-190S; LI-COR Inc.) mounted inside at the top of the plant chamber. Plants were in the measurement chamber for about 10 s for Exp. 2A and for about 35 s for Exp. 2B. During this time the CO2 concentration decreased about 10 µmol mol-1 for Exp. 2A and 15 µmol mol-1 for Exp. 2B, the relative humidity increased about 2% for Exp. 2A and 4% for Exp. 2B, and air temperature increased about 0.23°C for Exp. 2A and 0.25°C for Exp. 2B.

After CO2 assimilation measurements, shoots were harvested for leaf area and dry weight. The shoot was cut at the soil surface and partitioned for separate measurements of leaf area as well as leaf blade, leaf sheath, and stem dry weight. Leaf blades were separated from the sheath at the ligule and measured with a LI-3000 portable leaf area meter (LI-COR, Inc.). Shoot organs were then dried in a 60°C forced air oven to a constant weight that was recorded. In Exp. 2, shoot CO2 assimilation on a leaf area basis was determined by dividing shoot CO2 assimilation measurements by the leaf area measurements for each plant.

Root System Measurements
After leaf and shoot measurements were completed, root system characteristics were measured for all experiments. Root systems were removed from the pots, soaked in a water bath for 1h, suspended over a 0.7-cm sieve, and washed free of soil using a gentle stream of water. Root volumes were measured using water displacement in graduated cylinders. In Exp. 1A, total root system volume was measured. In Exp. 1B and Exp. 2, specific nodes of adventitious root axes were separated from the stem and their volume measured. In Exp. 2, the numbers of root axes per node and the lengths of those axes were also recorded.

Statistical Analysis
Data on root and shoot characteristics as well as CO2 assimilation and stomatal conductance were analyzed with ANOVA procedures in SAS (SAS Institute, 1996). With the occurrence of a significant ANOVA , means were separated by Duncan's Multiple Range Test (Little and Hills, 1978). Where treatment data did not conform to a normal frequency curve (e.g., root nodes totally removed by larval feeding), we deleted that data from the data set before ANOVA analysis. Leaf CO2 assimilation data, as recorded with time (Exp. 1B), were analyzed within measurement dates by ANOVA procedures in SAS. With the occurrence of a significant ANOVA, least significant difference values were calculated (Little and Hills, 1978) and plotted.

Leaf area data from both runs of Exp. 2, when plotted on a leaf number basis, had the appearance of a polynomial function. To further investigate this relationship and to determine which leaf had the greatest area, a polynomial equation was fit to the leaf area data from each plant by the analyze function of SAS (SAS Institute, 1996). The first derivative of each polynomial where the slope = 0 was then determined. These data, which represent the leaf position on the stem with the largest area, were then subjected to analysis by ANOVA procedures in SAS. With the occurrence of a significant ANOVA , means were separated by the least significant difference option (P.D. Evenson, 1998, personal communication).


   Results
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
Discussion and conclusion
 REFERENCES
 
Experiment 1
Plant Morphology
Plant growth was uniform across all treatments prior to rootworm larval feeding damage or mechanical damage to roots. In both runs of the experiment, the 150 larvae per pot treatment caused plants to have poor anchorage to the soil. Stems were given mechanical support to guard against lodging. With the exception of the 3-cut treatment in Exp. 1A, plants from all treatments appeared to be fully turgid and to have equal leaf development throughout both experiments. The 3-cut treatment in Exp. 1A caused plants to wilt and growth to stop.

Root Damage Effects on Tassel Stage Plants
In Exp. 1A, the 1-cut mechanical damage treatment removed about 30% of the root system while the 3-cut treatment removed about 75% when compared with the control treatment (Table 2) . These root volume changes were the result of mechanical damage to the seminal as well as the 1st through 5th nodes of root axes. Root damage caused by rootworm larval feeding, which reduced total root volume about 75% when compared with control at both infestation rates, was confined to the 4th and 5th root nodes.


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  		Table 2 Influence of western corn rootworm larval feeding and mechanical root damage upon total root system volume, ear leaf CO2 assimilation, and ear leaf stomatal conductance. Measurements were taken at the VT leaf stage {dagger} (354 soil GDD, 54 d after planting){ddagger}

 
Both mechanical damage treatments as well as both rootworm infestation treatments caused significant reductions in leaf stomatal conductance when compared with control plants (Table 2). The stomatal conductance in the 3-cut treatment was also significantly less than that seen in the other root damage treatments. These results confirm the observations of Riedell (1990) who found that mechanical cutting of roots and rootworm larval feeding damage significantly reduced leaf stomatal conductance when measured at the tassel development stage. However, even with these significant changes in total root volume and leaf stomatal conductance, the root damage caused by mechanical and larval feeding treatments (with the exception of the 3-cut treatment) had no significant effect on leaf CO2 assimilation when compared with the control treatment. It was only under the 3-cut treatment, which caused severe plant stress as evidenced by leaf wilting, that significant reductions in leaf CO2 assimilation were recorded.

Plant Responses during Root Damage
In Exp. 1B, root system mechanical damage was applied in a manner that would mimic the spatial and temporal characteristics of rootworm larval feeding damage. Pots were infested 38 d after planting (V7 leaf stage) with 2nd stage larvae. Sampling of extra pots revealed that late 3rd stage larvae and pupae were present in this experiment at 49 d after planting (V10 leaf stage). Mechanical damage treatments were performed on the 4th and/or 5th root nodes 45 d after planting (V9 leaf stage) and again on the 6th node 51 d after planting (V11 leaf stage). Plants harvested at the end of this experiment (VT stage, 589 soil GDD, 63 d after planting) revealed that mechanical root damage and larval infestation treatments had no significant effects on the volumes of the first 3 nodes of root axes (Table 3) . When compared with control plants, the 4th and 5th root node volumes were significantly less in the 4th node and above mechanical damage treatment as well in the 50 larvae per pot treatment. The 50 larvae per pot treatment resulted in the complete removal of the 4th and 5th root nodes while the 5th and 6th node mechanical cut treatment resulted in the complete removal of the 5th root node. Complete removal of specific nodal root axes by rootworm larval feeding, which has been previously reported in greenhouse experiments (Riedell, 1989), probably is a result of our infestation protocol which places 2nd stage larvae in close proximity to the base of the plant.


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  		Table 3 Influence of western corn rootworm larval feeding and mechanical root damage on the volume of specific nodes of adventitious root axes. Plants were harvested for root systems measurements at the VT leaf stage (589 soil GDD, 63 d after planting){ddagger}

 
Leaf CO2 assimilation measurements, performed on the youngest leaf with a ligule (Ritchie et al., 1992), revealed no significant differences between treatments on the first three sample dates (Fig. 1) . Pots were infested with 2nd stage larvae on Day 38. Thus, larval feeding damage which occurred during the first week of infestation had little effect on leaf CO2 assimilation. Because mechanical damage to the 4th and 5th root nodes was performed 45 d after planting and because late 3rd stage larvae and pupae were found 49 d after planting, measurements made 46 and 48 d after planting should be indicative of leaf CO2 assimilation levels in plants with recently-damaged roots. Plants treated with 150 larvae per pot or mechanical damage on the 5th and 6 node had significantly lower leaf CO2 assimilation than did control plants on both of these sample dates. The 50 larvae per pot and the 4th node and above mechanical cut treatments had values that were intermediate between the control and these treatments. There were no significant treatment effects at the 50 d after planting mark. The second round of mechanical cuts to the 6th node (performed 51 d after planting) as well as rootworm larval infestation, however, resulted in significantly lower CO2 assimilation compared with control plants 53, 55, and 58 d after planting. On the final measurement date when the plants were in the VT development stage, leaf CO2 assimilation in the 50 larvae per pot and the 5th and 6th node mechanical damage treatments were not significantly different than the control. In contrast, the 150 larvae per pot and the 4th node and above mechanical damage treatments resulted in CO2 assimilation measurements that were significantly less than the control at this date.



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  		Fig. 1 CO2 assimilation of the youngest leaf with a ligule in maize plants with root system damage caused by corn rootworm larval feeding or by mechanical cutting. Pots were infested 38 d after planting (V7 leaf stage). Late 3rd stage larvae and pupae were found 49 d after planting (V10 leaf stage). Mechanical damage to the 4th and/or 5th root nodes was performed 45 d after planting (V9 leaf stage) and again on the 6th node 51 d after planting (V11 leaf stage). Data points represent means for 4 replicate measurements per treatment. Upon obtaining a significant ANOVA for data within dates, LSD values represented by error bars were calculated

 
Experiment 2
Plant Morphology
Plant growth prior to rootworm larval infestation was uniform, with no visible nutrient deficiency symptoms or developmental abnormalities in both experimental runs. Plants in the 0 and 30 larvae per pot treatments were indistinguishable during the 14 d between infestation and plant harvest. However, plants subjected to the 60 larvae per pot treatment grew more slowly than those in the other treatments and had root systems that exhibited poor anchorage to the soil. Stems were given mechanical support to guard against lodging.

Root System Characteristics
Visual examinations of root systems harvested at the V9 leaf stage (Exp. 2A) revealed that uninfested plants had prolific growth in the seminal root system and 1st through 4th adventitious root nodes; axes of the 5th root node were just beginning to proliferate. Root growth at the V12 leaf stage (Exp. 2B) was very similar, with the exception that the 5th root node axes had elongated while the 6th root node axes were just beginning to proliferate. For both runs of the experiment, the seminal root system and the 1st and 2nd nodes of adventitious root axes exhibited no symptoms of rootworm larval feeding damage. The combined volumes of these root organs, which ranged from 29 to 39 mL in Exp. 2A, and 15 to 21 mL in Exp. 2B, were not significantly different across treatments. Infestation treatments resulted in characteristic larval feeding damage consisting of root tunneling and pruning of specific nodal root axes. When measured at the V9 leaf stage, the 30 larvae per pot treatment caused root pruning and shorter lengths of root axes on the 4th node compared to the control plants (Table 4) . The 60 larvae per pot treatment resulted in reductions in root volume and root axes length in the 3rd and 4th nodes when compared with control plants. At the V12 leaf stage, the 30 larvae per pot treatment resulted in total root pruning on the 4th node of root axes. The 60 larvae per pot treatment resulted in reductions of root volume and length on the 3rd and 4th nodes of root axes when compared to control plants.


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  		Table 4 Influence of corn rootworm larval feeding damage upon maize adventitious root characteristics at the V9 leaf stage (Exp. 2A) or the V12 leaf stage (Exp. 2B)

 
In both runs of Exp. 2, there was compensatory root growth (Belsky, 1986) in response to for rootworm larval feeding damage. At the V9 leaf stage, the 30 and 60 larvae per pot treatments had increased volume, length, and number of root axes on the 5th node relative to control plants (Table 4). At the V12 leaf stage, the 30 larvae per pot treatment had increased volume, length, and number of root axes on the 5th node compared to control plants. This node was not damaged in the 30 larvae per pot treatment, but was considerably damaged in the 60 larvae per pot treatment. This result suggests that the 5th node in the 60 larvae per pot treatment also may have increased in growth only to be further damaged by the greater numbers of rootworm larvae present in this treatment. Increased root axis growth in the 6th node in plants given 60 larvae per pot was also observed (data not shown) but was not sufficient to penetrate the soil surface. Thus, increased root axes growth and development (increased root volume, root length, and root axes number) in the node immediately above the root node damaged by rootworm larvae was a common characteristic of compensatory growth observed across both runs of the experiment. Similar compensatory root growth in response to larval feeding damage has been previously described under greenhouse conditions (Riedell, 1989). The total root system volumes of uninfested plants (71 mL in Exp. 2A; 79 mL in Exp. 2B) and plants given 30 larvae per pot (89 mL in Exp. 2A; 83 mL in Exp 2B) were larger than in plants given 60 larvae per pot (62 mL in Exp 2A; 41 mL in Exp. 2B). The similarity in total root volume between the uninfested and the 30 larvae per pot treatments was due in part to the compensatory growth of axes in the 5th root node of infested plants.

Shoot Characteristics
Leaf blade dry weights, measured at the V9 and V12 leaf stages, were less in plants grown in the 60 larvae per pot treatment than in the control treatment (Table 5) . Leaf blade dry weights of plants in the 30 larvae per pot treatment did not differ from those of the control plants. Leaf sheath dry weights followed similar, but nonsignificant, trends. Stem dry weights were also less in plants grown in the 60 larvae per pot treatment than in the control plants at the V12 leaf stage. Stem dry weights in the 30 larvae per pot treatment were intermediate between the other two treatments. Stem dry weight measurements at the V9 leaf stage followed similar, but non significant, trends. These data indicate that plants having only one node of roots damaged by rootworm larvae (30 larvae per pot) plus compensatory root growth in the root nodes above the damaged node grow and develop shoot organs in a manner very similar to undamaged plants. Plants that have two nodes of roots damaged (60 larvae per pot) have slower shoot organ growth and development than undamaged plants.


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  		Table 5 Influence of corn rootworm larval feeding damage upon shoot characteristics of maize plants at the V9 leaf stage (Exp. 2A) or the V12 leaf stage (Exp. 2B)

 


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  		Fig. 2 Area of individual leaves from maize plants grown in Exp. 2. Leaves were measured at the V9 (Exp. 2A) or V12 (Exp. 2B) leaf stage. The soil was infested when plants were at the V6 leaf stage with 0, 30, or 60 larvae per pot. Data points represent mean ± standard error for 5 replicate measurements per treatment

 
In the maize plant, leaves higher up on the stem grow and develop at later dates than leaves on the lower portion of the stem (Ritchie et al., 1992). Individual leaf area increased to a maximum (near Leaf 7 in Exp. 2A; near Leaf 8 in Exp. 2B) and then decreased again (Fig. 2) . At the V9 leaf stage (Exp. 2A), areas for Leaves 3 to 6 were very similar among treatments. Areas for Leaves 7 to 13 diverged with treatments, however. The control plants showed the largest individual leaf areas, the 60 larvae per pot treatment showed the least, and the 30 larvae per pot treatment showed intermediate values. At the V12 leaf stage (Exp. 2B), Leaf 5 in the 60 larvae per pot treatment had slightly larger leaf areas than the other treatments, while younger leaves (Leaf 8 and above) followed a trend similar to that observed in plants sampled at the V9 leaf stage.

These data indicated that damage to roots caused by larval feeding affected leaf area in a differential manner depending on the severity of damage and on leaf position on the stem. Visual evaluation suggested that leaf area data in Fig. 2 resembled polynomial functions. Polynomial equations for the leaf area data from each plant were generated by the analyze procedure in SAS. The regression fit r2 values for these polynomial equations were never less than 0.83 with most falling in the 0.95 to 0.97 range. The leaf number that had the greatest leaf area for each plant was calculated from the first derivative of these polynomial equations where the slope = 0. Statistical analysis of this data revealed that the leaf number having the maximum leaf area was not significantly different in the control and the 30 larvae per pot treatments, but was significantly less in the 60 larvae per pot treatment when compared with the control or the 30 larvae per pot treatments (Table 5). Taken together, these results support and extend the findings of Riedell (1989) and Gavloski et al. (1992) that severe rootworm larval feeding damage reduced shoot organ growth and development on the upper portion of the plant.

Shoot CO2 Assimilation
We measured the impact of root feeding on shoot CO2 assimilation on a per plant basis as well as shoot CO2 assimilation on a leaf area basis. In both runs of the experiment, shoot CO2 assimilation of whole plants was significantly less in the 60 larvae per pot treatment in which plants that had two nodes of root axes damaged with little compensatory root growth than in the control treatment (Table 6) . Leaf area in the 60 larvae per pot treatment was also significantly less than the control. At the V9 leaf stage, shoot CO2 assimilation in the 30 larvae per pot treatments, in which plants had one node of root axes damaged with compensatory root growth, were intermediate between the 60 larvae per pot treatment and the control. At the V12 stage, shoot CO2 assimilation in the 30 larvae per pot treatment was not different from control plants but was significantly greater than the 60 larvae per pot treatment. Leaf area at the 30 larvae per pot treatment was intermediate between the control and the 60 larvae per pot treatments for both experimental runs. However, there were no significant differences in shoot CO2 assimilation per unit of leaf area across treatments for both runs of the experiment.


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  		Table 6 Influence of corn rootworm larval feeding damage upon maize leaf area and CO2 assimilation in V9 leaf stage (Exp. 2A) or V12 leaf stage (Exp. 2B)

 

   Discussion and conclusion
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
 Discussion and conclusion
REFERENCES
 
It has been proposed that corn rootworm larval feeding damage affects maize plant physiology by disrupting crop water balance which in turn reduces plant turgor (Owens et al., 1974; Spike and Tollefson, 1989). This hypothesis implies that the greatest crop physiological stress imposed by larval feeding should occur after the larval population has reached the non-feeding pupal stage. At this time of maximum root damage, the plant would be lacking adequate root system size and morphology to provide sufficient water to the shoot (Riedell, 1990). In Exp. 1A, rootworm larvae reached the pupal development stage at about the time the plants were in the V12 leaf stage (505 soil GDD, 48 d after planting). Root system size, ear leaf CO2 assimilation, and ear leaf stomatal conductance measurements were taken 6 d after maximum root damage when the plants were in the tassel development stage. As in previous experiments (Riedell, 1990), we found significant reductions in root system size and leaf stomatal conductance under both larval infestation treatments when measured at this time. However, we found no significant larval root damage effects on ear leaf CO2 assimilation. These results confirm the findings of Godfrey et al. (1993a) and Hou et al. (1997) that rootworm larval feeding damage had no significant effects on leaf CO2 assimilation when measured at the end of the larval feeding period. Larval feeding damage effects on leaf CO2 assimilation, therefore, appear to be an exception to the generalization that shoot physiological parameters are most affected by corn rootworm larval feeding immediately after maximum root damage has occurred. Thus, our data as well as the data of others (Gavloski et al., 1992; Godfrey et al., 1993a; Hou et al., 1997; Riedell, 1990) suggest that the physiological stress response mechanisms triggered by rootworm larval feeding damage may be more complex in nature than proposed by Owens et al. (1974) and Spike and Tollefson (1989).

Viewing Exp. 1B data in a time course manner reveals that leaf CO2 assimilation (measured on the youngest leaf with a ligule) was significantly reduced during the time when larvae were damaging the root system or when specific root node axes were mechanically removed from the root system. These results confirm the observations of Godfrey et al. (1993a) and Hou et al. (1997) who found significant reductions in leaf CO2 assimilation during the initial period of larval feeding damage which coincided with the presence of first and second stage rootworm larvae. Our results show that leaf CO2 assimilation reduction gradually ameliorated after the insect population reached the non-feeding pupal stage (about Day 55) until the plants reached the tassel stage of development (Day 63) in plants with moderately damaged root systems (Fig. 1). This amelioration after feeding damage may explain earlier results showing no effect of root feeding on leaf CO2 assimilation.

Under field conditions, when plants had larval root damage of one node or less destroyed, Godfrey et al. (1993a,b) found that there were no significant differences in leaf area, leaf dry weight, or leaf CO2 assimilation at the time of maximum root damage (V10–V12 leaf stage). Hou et al. (1997) also found no significant effects of larval feeding (less than one node of root axes destroyed) on leaf and stem dry weight or leaf CO2 assimilation density when measured at the time of maximum root damage (V10–V14 leaf stage). Our data from Exp. 2 confirm the observations of Godfrey et al. (1993a,b) and Hou et al. (1997) in that plants with 1 node or less of roots damaged (our 30 larvae per pot treatment) compensated for larval root damage by increasing the growth and development of undamaged root axes in nodes directly above the damaged root nodes. This compensatory root growth was significant and likely contributed to maintenance of rapid shoot growth resulting in leaf dry weights, leaf areas, and shoot CO2 assimilation measurements that were not significantly different than those of uninfested plants. Godfrey et al. (1993a,b) and Hou et al. (1997) did not include experimental treatments that destroyed 2 nodes of root axes. Thus, it is difficult to extrapolate how plants might have responded to this level of damage under their experimental conditions. Our data indicate that severe larval feeding damage (more than one node of root axes destroyed) plus lack of compensatory root growth causes reductions in shoot growth, leaf area, and CO2 assimilation. Taken together, the data from our experiments suggest that the root damage severity plus the level of compensatory root growth play important roles in mediating shoot growth and CO2 assimilation responses to the stress imposed by corn rootworm larval feeding.

Plants often respond to stress by changing their hormonal balance (Chapin et al., 1988). Because certain plant hormones (cytokinins) are synthesized in the root tip (Feldman, 1984), changes in root structure and morphology could be instrumental in changing the biosynthetic capacity of root systems for cytokinin production (Riedell, 1989, 1993). A relationship between maize leaf photosynthetic activity and root cytokinin production has been demonstrated (Je2.gif" BORDER="0">ko and Vizárová, 1980; Je2.gif" BORDER="0">ko, 1981). Hormonal changes may act as the trigger that directly elicits reduced plant growth in response to stress (Chapin, 1991). Thus, it is tempting to postulate that the dramatic reductions in leaf CO2 assimilation during the time of larval feeding or mechanical damage to specific root nodes (Exp. 1B) as well as the reduced leaf area in younger leaves of severely damaged plants after larval feeding damage has ceased (Exp. 2) were initiated by reductions in the cytokinin levels produced by the damaged root systems. The present experiments, however, do not report any information that would help elucidate the actual hormonal mechanism(s) involved.


   ACKNOWLEDGMENTS
 
The authors thank D. Schneider for excellent technical assistance; B. Buman, B. Larson, and D. Nemitz for constructing the photosynthesis chamber; P. Evenson for statistical analysis; and T. Schumacher, L. Hammack, and J. Pikul for review of an earlier version of the manuscript. Mention of commercial or proprietary products does not constitute endorsement by the USDA. The USDA offers its programs to all eligible persons regardless of race, color, age, sex, or national origin.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
 Discussion and conclusion
 REFERENCES
 
Cooperative investigation between USDA-ARS and the South Dakota State Univ. Agric. Exp. Stn. Journal Series no 3100.

Received for publication October 1, 1998.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
 Discussion and conclusion
 REFERENCES
 




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