Evaluation of Pea and Soybean as Trap Crops for Managing Heterodera glycines

Trap crops that stimulate nematode egg hatching but not reproduction have been reported as an effective means for managing certain nematodes. Studies were carried out at two field sites each year in 1998 and 1999 to evaluate the potential of trapping the soybean cyst nematode (Heterodera glycines) with soybean and pea in the corn year to manage the nematode in Minnesota. The trap crops were planted on the same day as corn at each site and later killed with the herbicide glyphosate. Nematode egg densities were determined at planting, 1 and 2 months after planting, and at harvest. Treatments included four seeding rates (0, 124,000, 247,000, and 494,000 seeds/ha) of resistant soybean as a trap crop and four kill dates (3, 4, 5, and 6 weeks after planting). No effects of the trap-crop and kill-date treatments on H. glycines population density, corn yield, and the followingyear soybean yield were observed at the two locations. In a second study, the experiment included four trap-crop comparisons (resistant soybean at 494,000 seeds/ha, susceptible soybean at 494,000 seeds/ha, pea at 1,482,000 seeds/ha, and no trap crop) and five kill dates (3, 4, 5, 6 weeks after planting, and no-kill). At the Waseca site, egg density at harvest was lower where resistant soybean was grown for 6 weeks and where pea was grown for 5 and 6 weeks compared with where no trap crop was grown. Maintaining pea plants for more than 5 weeks, however, reduced corn yield by 20% at the Waseca site. At the Lamberton site, egg density at harvest was lower where the susceptible soybean was grown for 5 weeks compared with where no trap crop was grown. Even with significant reduction of eggs in some treatments, use of soybean and pea as trap crops in the corn year was not an effective means for managing H. glycines.     

Management of Heterodera glycines by Cropping and Cultural Practices

Heterodera glycines was identified in North Carolina in 1954, although symptoms of the disease were noted in the state at least 8 years earlier. Crop rotation experiments designed to develop management systems were initiated in 1956. Two or more years in production of a nonhost crop resulted in decreases of the nematode to low or undetectable levels with acceptable subsequent yields of soybean (Glycine max). Because of almost complete dependence on resistant cultivars and (or) nematicides for nematode control, crop rotation experiments were not conducted from 1962 to 1980. Research on control of H. glycines, beginning in 1981, emphasized biological and ecological aspects of the nematode in order to determine cropping systems that restrict the nematode to nondamaging levels. Mortality during embryogenesis was high at temperatures above 30 C. Hatching of eggs occurs readily in May and June. Postinfection development takes 2-3 weeks at weekly mean temperatures of 22-29 C and is slow above and below those temperatures. Egg production is high during the late growing season. Some cultural practices such as planting early maturing cultivars in mid-to-late June and rotation with a nonhost effectively keeps populations at low levels.     

Population Density and Spatial Pattern of Heterodera glycines in Relation to Soybean Phenology

Population dynamics of Heterodera glycines (SCN) were influenced by initial nematode population density in soil, soybean root growth pattern, soil type, and environmental conditions in two field experiments. Low initial populations (Pi) of SCN increased more rapidly during the growing season than high Pi and resulted in greater numbers of nematodes at harvest. Egg and juvenile (J2) populations increased within 2-6 weeks after planting when early-season soil temperatures were 20 C and above and were delayed by soil temperatures of 17 C or below in May and early June. Frequencies of occurrence and number of nematodes decreased with increasing depth and distance from center of the soybean row. Spatial pattern of SCN paralleled that of soybean roots. Higher clay content in the subsoil 30-45 cm deep in one field restricted soil penetration by roots, indirectly influencing vertical distribution of SCN. Shoot dry weight was a good indicator of the effect of SCN on seed yield. Root dry weight was poorly correlated with soybean growth and yield. The relationship of yield (seed weight) to Pi was best described by a quadratic equation at one site, but did not fit any regression model tested at the second site.     

Population Dynamics of Heterodera glycines in Conventional Tillage and No-Tillage Soybean/Corn Cropping Systems

The effects of no-tillage (NT), conventional tillage (CT), and crop rotation on soybean yield and population dynamics of Heterodera glycines were compared during a 7-year study in a silty clay loam soil with 6% organic matter. Either H. glycines-resistant ''Linford'' soybean or susceptible ''Williams 82'' soybean was rotated with corn and grown on 76-cm-wide rows in both tillage systems. Soybean was planted in 1994, 1996, 1998, 1999, and 2000. Yield of Linford was significantly greater than Williams 82 in all years. Soybean yield was affected by tillage in 1999 and 2000. No-tillage production tended to support more reproduction (R = number of eggs at harvest/number of eggs at planting) on both cultivars. The largest R for Williams 82 were in 1998: 58.35 for NT plots and 11.78 for CT plots. For Linford, the largest R were 12.09 for NT plots in 1996, and 3.71 for CT in 1999. When corn was planted, R decreased more in NT. When soybean was planted in years subsequent to 1994, numbers of eggs at harvest (Pf) were greater for Williams 82 NT than for Williams 82 CT or Linford in both tillage systems; however, crop rotation with corn negated these population increases. The soil became suppressive to H. glycines in 1999 and was suppressive in 2000. After the 3 years of continuous soybean, Pf per 250 cm[sup3] soil were 2,870 for Williams 82 NT, 791 for Williams 82 CT, 544 for Linford NT, and 990 for Linford CT in 2000, compared with Pf of 13,100 for Williams 82 NT, 15,000 for Williams CT, 2,360 for Linford NT, and 2,050 for Linford CT in 1994. Describing population dynamics solely on the basis of R was not adequate, but also required independent examination of initial populations following overwintering and Pf after the growing season. Planting soybean either NT or CT in rotation with corn did not result in long-term increases in numbers of H. glycines eggs.     

Effect of the rhg1 Gene on Population Development of Heterodera glycines

The effect of the rhg1 gene on equilibrium population densities (E) and reproduction factors (Rf) of Heterodera glycines was studied by comparing the nematode population development on two near-isogenic soybean lines (NIL), differing at the rhg1 locus. The NIL were inoculated with a series of initial egg densities (Pi) in the greenhouse. The relationships between final population densities (Pf = females per plant or eggs per plant) or Rf (final egg density/Pi) on both NIL and Pi were adequately described by quadratic models. The rhg1 gene suppressed Pf and Rf at all Pi of a population of H. glycines race 3 (HG Type 0-); E and maximum Rf were higher on the NIL-S line than on the NIL-R line. After two generations of culture of the race 3 population on the NIL-R line, the population selected by the rhg1 gene (R-eggs) had higher Pf and Rf on the NIL-R line than the population cultured on the NIL-S line (S-eggs) at all Pi. Both R-eggs and S-eggs produced similar egg numbers on the NIL-S line, which was higher than the egg number of either population on the NIL-R line at all Pi. The ratio of E in female numbers on the NIL-R line to E on the NIL-S line increased from 29% for the original race 3 population (S-eggs) to 46% for the rhg1-selected population (R-eggs). Regardless of different egg sources, a trend of increase in the number of eggs per female with the rise of Pi was observed on the NIL-S line. In contrast, female fecundity of both populations declined with the increase of Pi on the NIL-R line. At most inoculum densities, the highest number of eggs per female was observed on the NIL-S line inoculated with the R-eggs, whereas the lowest number of eggs per female was detected on the NIL-R line inoculated with the S-eggs. This study demonstrated that the E and maximum Rf determined by the quadratic models are useful measurements of plant resistance to nematodes.     

Multivariate Analysis of Selected Edaphic Factors and Their Relationship to Heterodera glycines Population Density

The influence of selected soil physical and chemical factors on population density of Heterodera glycines was investigated in 1988 and 1989 in two different locations of a soybean (Glycine max) field. Soil variables of a Norfolk loamy sand were measured after planting soybeans susceptible to H. glycines. Cyst and egg populations were determined after harvest. Nematode population density was found to be clustered. Up to 91% of the eggs were parasitized by a sterile fungus. Principal component analysis with orthogonal VARIMAX rotation grouped 12 variables into five uncorrelated factors in 1988 and three in 1989. In 1988, the factor "pH and Mg" was positively correlated (P < 0.001) with cyst and egg population density. Also, the factor "fine texture and Cu" was negatively correlated (P < 0.05) with egg population density. In 1989, the factor "pH, Mg and Cu" was positively correlated (P < 0.05) with levels of cysts and percentage of parasitized eggs, but not with total egg number. Across 2 years, factors containing soil pH and Mg were positively associated with cyst nematode population density. Copper appeared to be negatively associated with populations of H. glycines.     

Overwinter Population Dynamics of Heterodera glycines

The purpose of this research was to compare the overwinter survival of populations of Heterodera glycines at different latitudes in the United States and the effect of changing latitudes before and after the initiation of dormancy. Soil samples infested with H. glycines were collected in August or October in 1992 to 1994 from soybean fields in two to four states (combinations of Arkansas, Florida, Minnesota, Missouri, and Wisconsin). The samples were mixed thoroughly, divided into subsamples, shipped to an overwinter location, and buried until time for processing. To determine survival, cysts, eggs, and second-stage juveniles were extracted from replicated subsamples and counted each month from December to May. Survival generally was between 50% and 100%, and often was best in the state of origin. In Florida, survival was at the 50 to 100% level in soil from most locations, and in Wisconsin was near 100%. Survival of H. glycines in Arkansas and Missouri varied more than at the other locations. In a separate test, survival in microplots in Arkansas, in a more natural environment than that of buried samples, was 70 to 94% for field isolates from Arkansas, Minnesota, and Missouri and 100% for isolates of races 1, 3, and 14 that had been maintained in a greenhouse for several years. Survival appears to be better than previous tests had indicated. High survival rates require cultivars with high levels of resistance and long-term rotations for management.     

Variability in Host Preference Among Field Populations of Heterodera glycines

Eighteen soybean fields, six each with race 3, race 4, or Bedford population of Heterodera glycines, were selected for testing of host variability. Each field was divided into three sections, and a bulk soil sample was taken from each section. The 54 bulk soil populations (BSP) and 270 single cyst populations (SCP) were subjected to race determination tests. Tests of the 18 BSP and 90 SCP from the race 3 fields revealed that race 3 was the predominant race; however, 68 of the populations tested were other races. Tests of the 18-BSP and 90 SCP from race 4 fields demonstrated that races 2 and 4 were predominant, with 38 and 39 populations; respectively. Tests of the 18 BSP and 90 SCP from the Bedford population fields revealed tremendous variability. Races 2, 4, and 6 were the predominant races, with 32, 31, and 28 populations, respectively. These results indicate that of the three races studied, the Bedford population is the most variable, race 3 shows considerable variability, and race 4 shows very little.     

Tolerance of Soybean to Heterodera glycines

Seven soybeans were selected from 200 entries evaluated for tolerance to soybean cyst nematode (SCN), Heterodera glycines. Tolerance to SCN was measured by comparing the seed yield from aldicarb-treated vs. nontreated plots. A yield response index (YRI) was calculated for each entry: YRI = (seed yield from nontreated plot/seed yield from treated plot) × 100. The soybean entries Coker 156, PI 97100, and S79-8059 exhibited high tolerance (YRI) to SCN when compared to Essex even though they became heavily infected with SCN. Tolerance in soybeans to SCN may be useful in pest management programs designed to stabilize soybean yield.     

Heterodera glycines in Indiana: I. Reproduction of Geographical Isolates on Soybean Differentials

Four of five geographical isolates of Heterodera glycines from Indiana classified as Race 3 using standard differentials showed many differences when classified using another group of differentials comprised of five soybean breeding lines and cultivars. Two isolates from northern Indiana produced cysts on more of the differentials tested than did three isolates from southern Indiana, suggesting that potential resistant lines should be tested on a range of H. glycines populations originating from the areas for which cultivars are being developed.     

Coating Soybean Seed with Oxamyl for Control of Heterodera glycines

Oxamyl coated on soybean (Glycine max (L.) Merr. cv. Elgin) seeds in solutions of 20, 40, 80, and 160 mg/ml had no serious deleterious effects on seedling emergence and growth when planted in sterile soil. Seedling emergence on day 3 was less than that of the uncoated control, but by day 7 emergence was equal to, or greater than, the control. Shoot and root growth from seed coated with oxamyl in 40 and 80 mg/ml solutions was greater than that of the control. In soil infested with soybean cyst nematode, Heterodera glycines, shoot weight of soybean plants from seeds coated with oxamyl in 80 mg/ml solution was 11 and 9% greater at weeks 3 and 7, respectively, than from uncoated seeds. Numbers of juveniles (J3 and J4) and adults of H. glycines observed on the roots of plants from oxamyl-coated seeds were 83, 42, and 49% less at weeks 3, 5, and 7, respectively, than numbers on the roots of the untreated control. Numbers of J2 extracted from the roots of plants from oxamyl-coated seeds were 75% less at weeks 5 and 7 than those extracted from roots of uncoated seeds. The numbers of J2 extracted from the soil planted to oxamyl-coated seeds were 51 and 33% less at weeks 5 and 7, respectively, than from soil planted to uncoated seed.     

Influence of Temperature and Soybean Phenology on Dormancy Induction of Heterodera glycines

Growth room and field experiments were conducted to determine the influence of soil temperature and soybean phenology on dormancy induction of a North Carolina population of Heterodera glycines race 1. Three temperature regimes and two photoperiods to regulate plant phenology were investigated in growth rooms. H. glycines hatch was greatest from the 26 and 22 C (day and night) temperature treatment, intermediate at 22 and 18 C, and least from the decreasing regime (26 and 22 C, 22 and 18 C, and 18 and 14 C). More eggs hatched and greater nematode reproduction occurred on pod-producing soybeans than on those that remained vegetative. In the field study, hatching patterns were not different between depodded and naturally senescing soybeans nor between the different maturity groups of soybean cultivars (groups V through VIII). Egg hatch (9-16%) was greatest in August and September when mean soil temperatures were between 25 and 29 C. Hatch declined to 1% in vitro and was not detectable in the bioassay in November. Greatest nematode numbers were observed on the latest maturing cultivar (group VIII) and fewest on the cultivar which matured earliest (group V). Decreasing temperature appears to be more important than soybean phenology in dormancy induction of H. glycines.     

A Technique for Evaluating Heterodera glycines Development in Susceptible and Resistant Soybean

A technique was developed to evaluate Heterodera glycines development in susceptible and resistant soybean. Roots of 3-day-old soybean were exposed to infective juveniles of H. glyci.nes in sand for 8 hours followed by washing and transfer to hydroponic culture. The cotyledons and apical meristem were removed and plants were maintained under constant light, which resulted in a dwarfed plant system. After 15 or 20 days at 27 C, nematodes were rated for development. Emerged males were sieved from the culture water and females were counted directly from the roots. Nematodes remaining in the roots were rated for development after staining and clearing the tissues. The proportion of nematodes at each stage of development and the frequency of completed molts for each stage were calculated from these data. This technique showed that resistance to H. glycines was stage related and did not affect males and females equally in all resistant hosts. The resistance of plant introduction PI 209332 primarily affected development of third and fourth-stage juveniles; ''Pickett'' mainly affected second and third-stage juveniles, whereas PI 89772 affected all stages. Male development was markedly affected in PI 89772 and ''Pickett'' but not in PI 209332.     

Dormancy of Heterodera glycines in Missouri

A 2-year study was conducted in field microplots to determine the relative importance of soybean phenology and soil temperature on induction of dormancy in Heterodera glycines in Missouri. Four near-isogenic soybean lines differing for maturity date were planted in microplots infested with a race 5 isolate of H. glycines. Soil temperature was monitored at a depth of 15 cm. Eggs of H. glycines, extracted from cysts collected monthly from each microplot, were used in hatching tests and bioassays to determine dormancy. Egg hatching and second-stage juvenile (J2) infectivity rates decreased sharply from their highest levels in midsummer (July-August) to a low level by October of each year and remained low (< 10% hatching and < 0.2 J2/cm root) until May or June of the following year. The patterns of numbers of females and eggs in the bioassays were similar. The decreases were not related to soil temperature and did not differ consistently among soybean isolines. The monophasic changes in all nematode responses with peak midsummer rates suggest that H. glycines produces one primary generation per year in central Missouri. Changes in hatching rates and the timing of minimum and maximum rates suggested that H. glycines eggs exhibit more than one type of dormancy.     

Impact of Herbicides on Heterodera glycines Susceptible and Resistant Soybean Cultivars

Several abiotic and biotic stresses can affect soybean in a growing season. Heterodera glycines, soybean cyst nematode, reduces yield of soybean more than any other pathogen in the United States. Field and greenhouse studies were conducted to determine whether preemergence and postemergence herbicides modified the reproduction of H. glycines, and to determine the effects of possible interactive stresses caused by herbicides and H. glycines on soybean growth and yield. Heterodera glycines reproduction factor (Rf) generally was less on resistant than susceptible cultivars, resulting in a yield advantage for resistant cultivars. The yield advantage of resistant cultivars was due to more pods per plant on resistant than susceptible cultivars. Pendimethalin reduced H. glycines Rf on the susceptible cultivars in 1998 at Champaign, Illinois, and in greenhouse studies reduced dry root weight of H. glycines-resistant and susceptible cultivars, therefore reducing Rf on the susceptible cultivars. The interactive stresses from acifluorfen or imazethapyr and H. glycines reduced the dry shoot weight of the resistant cultivar Jack in a greenhouse study. Herbicides did not affect resistant cultivars'' ability to suppress H. glycines Rf; therefore, growers planting resistant cultivars should make herbicide decisions based on weeds present and cultivar tolerance to the herbicide.     

Effects of Biosolid Soil Amendment on Heterodera glycines Populations

The high degree of parasitic variability in Heterodera glycines and its distribution in a wide range of soybean production systems present multiple challenges for management, which necessitate increased understanding of the biology of H. glycines. Soil amendments are being considered either as stand-alone and/or as part of integrated management approaches. A recycled municipal biosolid with nutrition supplement and liming qualities, N-Viro Soil (NVS) has potential as a multi-purpose soil amendment. In three greenhouse experiments, the effects of 0, 1.0 or 4.0 g NVS/100 cm³ of sandy loam soil on three H. glycines populations (GN1, GN2 and GN3) were investigated on soybean grown for 557 ± 68 degree-days (base 10°C). The response of the three H. glycines populations to NVS treatment varied by experiment. The overall numbers of preadult stages and cysts generally decreased with increasing levels of NVS in all experiments, and the high rate was more effective than the low rate in suppressing H. glycines numbers. This suggests that the high NVS treatment can affect the three populations in the experimental soil type under controlled conditions. Field studies to determine efficacy of the soil amendment in a wide range of environments should be initiated.     

Variation in Resistance of Soybean Lines to Races of Heterodera glycines

The objective of this study was to determine the interrelationships of Heterodera glycines races based on their resistance to soybean (Glycine max) cultivars and lines against which they were tested. Greenhouse tests determined the numbers of females of each of eight races of H. glycines that developed on 277 to 522 soybean cultivars and lines. A Female Index (number of females on a test cultivar as a percentage of the number on ''Lee 74'') was calculated and used in frequency distributions, correlations, and duster analyses of the resistance reactions to the different races in an attempt to determine relationships among cultivars. Frequency distribution patterns of all cultivars and lines tested against each race were skewed in favor of resistance, and in some cases bimodality was observed. The majority of correlations between pairs of races were highly significant. Cluster analyses based on the correlations divided eight races into four clusters that explained 73% of the variation in resistance. Cluster 1 was comprised of races 2, 4, and 14; Cluster 2 was comprised of races 6 and 9; Cluster 3 was comprised of races 1 and 3; and Cluster 4 was comprised of race 5. The information obtained in this study could increase the efficiency of testing resistant soybean breeding lines for resistance to H. glycines.     

Effect of Liquid Swine Manure on Hatch and Viability of Heterodera glycines

Experiments were conducted in the laboratory and greenhouse to determine the effect of raw and anaerobically digested liquid swine manures on the hatch and viability of Heterodera glycines, the soybean cyst nematode. Anaerobic digestion was performed for 15 and 35 days to enrich volatile fatty acids (VFA) and ammonium (NH₄ ⁺), respectively. All filtrates of the raw, VFA-enriched, and NH₄ ⁺-enriched manures at 10⁻¹ to 250⁻¹ dilutions inhibited H. glycines hatch, and the reduction of hatch was increased with increasing concentration of the manure. Cumulative hatch at day 21 was only 2.1% to 3.7% in the 10⁻¹ dilution manures, while the hatch in water was 21% to 27.3%. The high concentrations appeared to be lethal to some eggs. Most second-stage juveniles (J2) of H. glycines were killed when incubated for 8 hours in the manure filtrate at the original concentration (>90% mortality) or for 48 hours at the 64⁻¹ dilution (> 82% mortality). When J2 were treated with the manures at 10⁻¹ to 250⁻¹ dilutions for 4 hours, only the 10⁻¹ dilution of VFA-enriched and raw manures resulted in a lower number of J2 that penetrated soybean roots as compared with lower concentrations. The VFA-enriched manure was the best, raw manure intermediate, and NH₄ ⁺-enriched manure the least effective in inhibiting H. glycines hatch and killing eggs and J2.