| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
a Monsanto Company, 3100 Sycamore Rd., DeKalb, IL 60115 USA
b Dep. of Entomology, Iowa State University, Insectary Bldg., Ames, IA 50011-3140 USA
stephen.a.lefko{at}monsanto.com
 |
ABSTRACT |
|---|
 TOPNOTES ABSTRACT INTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
Abbreviations: EIL, economic injury level • ET, economic threshold
|
INTRODUCTION |
|---|
|
TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
The potential for leafhopper-resistant alfalfa was first recognized in the 1980s when Sorensen et al. (1985, 1986) and Shade and Kitch (1986) released perennial alfalfa germplasm with multiple pest resistance. Releases were referred to as glandular-haired alfalfa, although the mechanism of resistance was not fully described. This reference to glandular hairs probably was because these releases had a phenotype similar to the alfalfa described by Shade et al. (1979), who showed that hairs on an annual alfalfa secreted a sticky substance that entangled small insects.
Researchers have investigated the presence and importance of antibiosis, the negative effect of a plant on the fitness of an individual; nonpreference, the characteristic(s) of a plant that make it an undesirable host; and tolerance, the ability of a plant to avoid injury while still supporting a pest; in perennial resistant alfalfa (Painter, 1951). Most studies have emphasized the importance of pubescence in conferring resistance. Brewer et al. (1986a) compared three species of resistant (glandular-haired) alfalfa with one susceptible type. Mortality was greatest on the resistant alfalfa, compared with the control, in no-choice experiments. However, most of the clones of resistant alfalfa showed feeding and ovipositional nonpreference when a susceptible host was available. The authors did not detect an entrapment mechanism similar to the one described by Shade et al. (1979) in annual glandular-haired types. In a separate study, Brewer et al. (1986b) described how highly lignified tissues might enhance resistance to the leafhopper.
Elden and Elgin (1992) performed free-choice and no-choice experiments on alfalfa having dense pubescence and resistance to multiple pests. They concluded that some clones had high levels of feeding and ovipositional nonpreference and nymphal antibiosis. Similarly, clones that were antibiotic in no-choice tests demonstrated nonpreference when alternate hosts were available. Their conclusions on nymphal and ovipositional nonpreference should be interpreted with caution. It appears the effect of adult (female) mortality and, consequently, total oviposition were unaccounted for and could be the cause of the variation in the number of nymphs produced on each line of alfalfa.
Elden and McCaslin (1997) conducted no-choice studies and showed a significant but weak correlation between the density of glandular hairs and resistance to potato leafhopper in 19 glandular-haired alfalfa clones. Estimates of nymphal mortality ranged from 0 to 33%; however, it is unclear if nymphal mortality data were corrected using adult (female) survival, which probably influenced total oviposition. They reported 13 to 96% mortality of adult leafhoppers in no-choice cage tests. They also stated that glandular hairs on perennial clones did not entrap leafhoppers and suggested that an unexplained resistance mechanism may exist. These studies using stem cuttings have been paramount to a better understanding of the mechanism of resistance. It is difficult, however, to extrapolate their results to field conditions without great uncertainty. Using these results, producers could expect suppressed leafhopper numbers; antibiosis would be overridden by nonpreference since alternate hosts would be available (Poos and Wheeler, 1943).
Hogg et al. (1998) and Lefko (1999) conducted comparative studies of adult and nymphal population size in field plots of glandular-haired and susceptible alfalfa cultivars. This type of study could be used only to reject the presence of plot-level nonpreference or implicate, but not differentiate between, antibiosis and nonpreference. Both reports showed the adult population density was similar between resistant alfalfa and the susceptible control(s). Hogg et al. (1998) found fewer nymphs in glandular-haired alfalfa; however, Lefko (1999) did not find these differences. Both studies concluded that nonpreference is an improbable explanation for the mechanism of resistance at a production scale.
While antibiosis and nonpreference have been the focus of most studies, tolerance has received little attention (Manglitz and Sorensen, 1999). This mechanism is important because Hogg et al. (1998) and Lefko et al. (1997) showed that the population density of potato leafhopper was similar between resistant and susceptible cultivars, yet there was a yield advantage in resistant alfalfa when the leafhopper densities were high.
Our objectives were to determine if alfalfa yield response to potato leafhopper feeding differs between resistant and susceptible alfalfa, and if the potato leafhopper population growth potential differs among field plots of resistant and susceptible alfalfa. Results would help determine if tolerance is an important mechanism, and if so, how pest management guidelines could accommodate it.
|
Materials and methods |
|---|
|
TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
A second experiment was initiated on 27 Apr. 1998 in a neighboring field on the same farm. Tolerant cultivars used in the experiment were 53V63, 54H69, and 3A09 (experimental line). The susceptible control again was 645. The former two tolerant cultivars were second commercial releases and probably provide better protection from potato leafhopper than earlier releases. These plots measured 1.5 by 7.4 m and were arranged according to a randomized complete block design, also using four replicates. This experiment was planted with a cultipacker-style cone planter calibrated to deliver seed at 16.9 kg/ha.
All alfalfa was harvested twice during the seeding year and three times during subsequent years. Alfalfa was harvested when it had visually reached the early to mid-bloom stage. Potato leafhoppers were caged on alfalfa to achieve different levels of pest pressure. Cages were constructed from plastic refuse containers that measured 70 cm tall by 52 cm in diameter at the open end (Fig. 1) . The opening covered a land area of 0.21 m2. The side panels and bottom were cut from the containers and 32-by-32 Lumite mesh (Synthetic Industries, Gainesville, GA) was attached in their place. Containers were reinforced on the inside with wooden lath and secured to the ground using tent stakes.
|
|
Nymph counts per cage were converted to an index of population growth to normalize values across all leafhopper densities. The conversion equation was
 |
Alfalfa dry weight and leafhopper density data were used to calculate yield-loss equations for each cultivar in each trial. Estimates of percentage loss were calculated for infested cages using the zero level of infestation in each plot as a basis. Least squares linear regression (SAS Inst., 1990) was used to calculate linear model coefficients. Linear models were fitted to average percentage loss values for each level of infestation according to treatment. Models were recalculated and forced through the origin if the original y-intercept was positive. This procedure was used to maintain biological meaning at the expense of statistical significance (r2), since a positive y-intercept indicates yield loss from the potato leafhopper when its number is zero. Differences between slopes and intercepts were tested in each trial using a Student's t-test performed on all pairwise combinations of alfalfa (Zar, 1984). The same procedure was used to test differences among slopes for 645, the susceptible control, among trials.
Economic injury levels were calculated using the equation
 |
|
Results |
|---|
|
TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
Index values <1 probably resulted from poor leafhopper control in cages before the trial, which resulted in nymph populations in uninfested cages. The average number of nymphs collected from uninfested controls, including tolerant and susceptible alfalfa, were from 5.3 to 9.0 nymphs per cage. High numbers would decrease the numerator in the conversion equation and result in smaller index values.
Yield-Loss Coefficients
Comparisons of linear model coefficients were made for all pairwise combinations of cultivars. Also, coefficients were compared among years for both alfalfa types. The slope of each model equals the percentage of yield loss per 0.21 m2 expected for each additional potato leafhopper. This coefficient is referred to as the loss rate throughout this paper. The loss rate is one variable used to calculate the EIL, and lower values result in higher ETs. Another important coefficient is the intercept of the linear model. The x-axis intercept is the pest number when loss begins.
There was a trend for lower loss rates and positive x-axis intercepts in tolerant alfalfa compared with the susceptible control; however, these differences were only detected in regrowth intervals after the initial growth of seedling alfalfa. Additionally, there was a trend for loss rates of all alfalfa to decrease as stands aged. Results in the following paragraphs are reported beginning with the trial performed on the youngest alfalfa and ending with the trial on the oldest alfalfa.
The trial performed on the initial (seedling) growth of tolerant alfalfa showed no trend for smaller loss rates in tolerant cultivars compared with the susceptible control (Table 1). The only statistical difference between loss rates was found between 53V63 and 645 (t = 2.83; df = 4; P = 0.05) and between 53V63 and 54H69 (t = 3.14; df = 4; P = 0.05). These differences are unimportant because large experimental error caused a negative, and probably meaningless, loss rate for 53V63. Both the control and 3A09 had positive x-intercepts; however, there was no statistical difference between these values.
The onset of resistance was first detected in the next trial that used the second cutting of a seeding-year stand. All loss rates for tolerant cultivars were less than the control in this trial (Table 1). The loss rates of AmeriGuard 301 (t = 5.49, df = 4, P = 0.05) and 5347LH (t = 5.61, df = 4, P = 0.05) were significantly lower than the control. Therefore, these tolerant cultivars had a significant yield advantage over the control at this age and within this range of pest pressure. Of the tolerant cultivars, Trailblazer had the highest loss rate (0.158); however, this loss rate was not significantly different from all other tolerant cultivars. Conversely, the regression fit to Trailblazer data had the highest x-axis intercept (38.86), although it was not statistically different from the others. Even though the yield advantage of tolerant alfalfa was detected at this plant age, the mechanism of resistance was not obvious because tolerant alfalfa had no measurable effect on nymphal production.
Levels of leafhopper infestation were doubled for tolerant alfalfa compared with susceptible alfalfa in the trial using the second cutting of second-year alfalfa (Table 1). This adjustment was necessary because of the relatively low loss rates in the previous trial. Surprisingly, the yield response was less evident in this trial than in the previous trial. Statistically, there were no differences in loss rates among cultivars. The loss rate of the control remained much higher. It was more than four times larger than the lowest loss rate of tolerant cultivars, even though twice as many leafhoppers were caged on tolerant cultivars. Only 5347LH had a positive x-axis intercept. Even though a yield advantage persisted in leafhopper-tolerant alfalfa, a negative effect on leafhopper population growth was absent (Table 1).
Levels of infestation were increased again in the next trial using second-cutting third-year alfalfa. The control infestation levels were 0, 40, 80, and 120 leafhoppers per 0.21 m2, and tolerant alfalfa had levels twice as high: 0, 80, 160, and 240 leafhoppers per 0.21 m2. Although the leafhopper number was twice as high in tolerant cages, there were no differences among loss rates for all cultivars. Again, this lack of difference suggests that tolerant cultivars outperformed the susceptible control by tolerating twice as many potato leafhoppers.
Another trend that emerged from this series of experiments was for loss rates to decrease (become more tolerant) with alfalfa age. This was especially obvious in the control (Table 2) . The loss rates for the control were 0.334 ± 0.224 and 0.613 ± 0.032, respectively, for the first and second cuttings of the seeding year. These values decreased to 0.095 ± 0.099 during the second year, and decreased again to 0.024 ± 0.068 during the third year. Pairwise t-tests of all combinations showed the seeding-year, second-cutting loss rate (0.613 ± 0.032) was significantly higher than loss rates from all other age classes. A conservative interpretation of these results is that the potential for alfalfa loss from potato leafhopper is probably different between the seeding year and years after.
|
|
Discussion |
|---|
|
TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
Painter (1951) described how the role of the plant was more important than the role of the insect when tolerance was the resistance mechanism. In this study, tolerance is the best explanation of the resistance mechanism. However, the important factor is the insect's response to the genetic variability in an alfalfa stand. Combining results from the present study with the feeding and sampling studies described earlier, stand tolerance is the best explanation of the resistance mechanism.
A mechanism that appeared antibiotic using no-choice tests and single stems may appear as nonpreference when susceptible hosts are available. Brewer et al. (1986a) and Elden and Elgin (1992) confirmed this. An alfalfa stand presents leafhoppers with a diverse array of feeding and oviposition locations because of its autotetraploid genetic characteristic (McCoy and Bingham, 1988). Therefore, while antibiosis and nonpreference may function among individual plants in a field, the fraction of suitable hosts in a tolerant stand may be great enough that the stand's carrying capacity remains unchanged. Hogg et al. (1998) and Lefko (1999) confirmed this in field studies.
Tolerance may best describe how these new cultivars respond to feeding from the potato leafhopper. Moreover, tolerance may function at the individual plant level, as Painter (1951) described it, or at the field level. Below are explanations of how tolerance may function at each level.
First, plant-level tolerance, or resistance to hopperburn (Jarvis and Kehr, 1966; Kindler et al., 1973), may exist in the alfalfa population, and its efficacy is likely variable among individual plants in a stand. One explanation is related to insect behavior. Hunter and Backus (1989) identified different feeding behaviors of the potato leafhopper and linked the symptoms with one feeding behavior (multiple-cell laceration and flush). It may be that the morphology of tolerant plants causes the leafhopper to change feeding behavior to one that is less damaging (Brewer et al., 1986b; Calderon and Backus, 1992). Another explanation is that tolerant plants may metabolize or be less receptive to the toxic compounds in leafhopper saliva that cause cell damage.
Field-level or stand tolerance can also be explained in at least two ways. Both explanations assume leafhopper damage is concentrated on suitable (less tolerant) plants in the alfalfa stand. First, the growth rate or form of tolerant plants may compensate for neighboring plants that are more attractive hosts and are consequently stunted by the leafhopper (Hutchins and Pedigo, 1989; Hutchins et al., 1990). Another explanation is that loss per potato leafhopper decreases as the number per plant increases. Leafhoppers remove assimilates, and enzymes deposited in vascular tissue during feeding cause damage (Ecale and Backus, 1995a, 1995b). Hower and Flinn (1986) described how the probability of feeding on previously damaged tissue increases with insect number and that loss per leafhopper nymph decreases as the nymph number per plant increases. Womack (1984) corroborated these findings in a physiological study; alfalfa photosynthesis and transpiration declined as the leafhopper number per stem increased. Therefore, the leafhopper population damage potential might be reduced if leafhoppers aggregate on a fraction of the stand.
Studies investigating the distribution of leafhopper symptoms in an alfalfa population could provide a more definitive explanation of stand tolerance. Additionally, the level of resistance (including nonpreference, antibiosis, and tolerance) will undoubtedly increase in future cultivars, and the fraction of suitable hosts in the stand will likely decline. Therefore, stand tolerance may be an artifact of the early stage of breeding for leafhopper resistance. It may be wise to predict the effect this change will have on the resistance mechanism and investigate the value of eliminating the fraction of the stand that will support a potato leafhopper population.
We propose the concept of stand tolerance in describing the reaction of the new glandular-haired alfalfa cultivars to potato leafhopper pressure. Stand tolerance implies the interplay of more than one resistance mechanism, but emphasizes the impact this tactic will have on pest management by raising the EIL.
Calculating EILs
Painter (1951) pointed out how ecologically compatible and practical host plant resistance is in pest control, and he identified tolerance as a premier mechanism. Later, Stern et al. (1959) explained how tolerance was unique from virtually every other pest management tactic, including other resistance mechanisms, because its objective was not to suppress the pest number. They theorized how tolerance would increase the EIL instead of suppressing the pest number below a tolerable level (Fig. 2)
. Results from this study show that stand tolerance creates a yield advantage great enough to warrant calculating separate EILs for susceptible and tolerant cultivars. Moreover, these data show that the ability to tolerate potato leafhopper changes with alfalfa age, and the rate of change may be different between tolerant and susceptible cultivars. We propose a two-step decision process for determining the optimal ET, depending on the type and age of the alfalfa stand (Fig. 3)
.
|
|
The loss rate for the susceptible control decreased greatly from the first and second cutting of the seeding year to the second cutting of the third year (Table 2). This difference may warrant the use of a higher ET. An ET of 33 leafhoppers per 10 sweeps was calculated using the yield-loss coefficients for the second cutting of the second year (y = 0.095x). This value is large compared with values described by Cuperus et al. (1983) (five adults per 10 sweeps) and DeGooyer et al. (1998) (11 adults per 10 sweeps). One explanation for this is that these previous studies did not account for stand age. A conservative ET may be between 8 and 33 adult leafhoppers per 10 sweeps for alfalfa after the seeding year.
A separate ET for tolerant cultivars was calculated using pooled results from 5347LH, AmeriGuard 301, and Trailblazer during the second cutting of the second year (y = 0.046x - 0.806). This value was 80 leafhoppers per 10 sweeps, and was 10 times larger than the earlier cutting of the same year and 2.4 times larger than the susceptible control in Year 2 (Fig. 3). Inclusion of third-year data would have increased the threshold to over 1800 leafhoppers per 10 sweeps. This number is unrealistically large, probably because the relationship between loss and leafhopper number is curvilinear, not linear, at such high densities.
Leafhopper-tolerant alfalfa cultivars may impact production in many ways. Results from this study showed it has a greater yield potential than susceptible alfalfa under leafhopper stress. This could increase alfalfa yield over the life of a stand without insecticides. Moreover, a higher ET should reduce the frequency of application and quantity of insecticide used for potato leafhopper management. This is shown in Fig. 4 , which uses leafhopper density data from Lefko (1999). The ET is exceeded in tolerant alfalfa only during the first cutting of 1996. The ET is exceeded in susceptible alfalfa during both cuttings in 1996 and the second cutting and early part of the third cutting in 1997. In this figure, the threshold for susceptible alfalfa is increased from 8 to 33 after the seeding year. If it had not been raised, the susceptible alfalfa would have spent even more time under economic loss conditions. The benefit of stand tolerance through a higher ET is clear.SAS Institute 1990
|
|
ACKNOWLEDGMENTS |
|---|
|
NOTES |
|---|
|
TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
Received for publication March 17, 1999.
|
REFERENCES |
|---|
|
TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResultsDiscussionREFERENCES |
|---|
This article has been cited by other articles:
|
|
 |
|
  E. A. Beckendorf, M. A. Catangui, and W. E. Riedell Soybean Aphid Feeding Injury and Soybean Yield, Yield Components, and Seed Composition Agron. J., February 26, 2008; 100(2): 237 - 246. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Ariss, L. H. Rhodes, R. M. Sulc, and R. B. Hammond Potato Leafhopper Injury and Fusarium Crown Rot Effects on Three Alfalfa Populations Crop Sci., July 30, 2007; 47(4): 1661 - 1671. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Hansen, J. E. Miller-Garvin, J. K. Waldron, and D. R. Viands Comparison of Potato Leafhopper-Resistant and Susceptible Alfalfa in New York Crop Sci., July 1, 2002; 42(4): 1155 - 1163. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. M. Sulc, E. van Santen, K. D. Johnson, C. C. Sheaffer, D. J. Undersander, L. W. Bledsoe, D. B. Hogg, and H. R. Willson Glandular-Haired Cultivars Reduce Potato Leafhopper Damage in Alfalfa Agron. J., November 1, 2001; 93(6): 1287 - 1296. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| The SCI Journals | Crop Science | Vadose Zone Journal | |||
| Journal of Natural Resources and Life Sciences Education |
Soil Science Society of America Journal | ||||
| Journal of Plant Registrations | Journal of Environmental Quality |
The Plant Genome | |||
