Effects of Cover Crops on Population Reduction of Soybean Cyst Nematode (Heterodera glycines)
- Krishna Acharya
- Guiping Yan †
- Addison Plaisance
- Department of Plant Pathology, North Dakota State University, Fargo, ND 58108
Microplot experiments were conducted to evaluate the effects of cover crops on population reduction of a major soybean pest, soybean cyst nematode (SCN; Heterodera glycines Ichinohe) in 2016 and 2017. Ten crop species, including annual ryegrass (Lolium multiflorum L.), Austrian winter pea (Pisum sativum L. subsp. arvense), carinata (Brassica carinata A. Braun), faba bean (Vicia faba Roth), foxtail millet (Setaria italica (L.) P. Beauvois), daikon radish (Raphanus sativus L.), red clover (Trifolium pratense L.), sweetclover (Melilotus officinalis L.), turnip (Brassica rapa subsp. rapa L.), and winter rye (Secale cereale L.), were planted along with susceptible soybean (Glycine max (L.) Merr. ‘Barnes’) in soil naturally infested with each of two SCN populations (SCN103 and SCN2W) from two North Dakota soybean fields. Crops were grown in large plastic pots for 75 days in an outdoor environment (microplot). Soil samples were collected from each pot for nematode extraction and SCN eggs were counted to determine the final SCN egg density. The population reduction was determined for each crop and nonplanted natural soil (fallow). All of the tested crops and nonplanted natural soil had significantly (P < 0.0001) lower final population densities compared with susceptible soybean (Barnes). Also, a significant difference (P < 0.0001) was observed between the SCN population suppressions caused by cover crops versus the fallow treatment. All cover crops except Austrian winter pea, carinata, faba bean, and foxtail millet had consistently lower SCN egg numbers than in fallow in both years of the experiments. The average population reductions of SCN by the cover crops ranged from 44 to 67% in comparison with the initial population density, while the fallow had natural reductions from 4 to 24%. Annual ryegrass and daikon radish reduced SCN egg numbers to a greater extent than the other cover crops, with an average of 65 and 67% reduction of initial population density, respectively, from 2 years. The results suggested that cover crops reduced the SCN populations in external microplot conditions, and their use has great potential for improving SCN management in infested fields.
The soybean cyst nematode (SCN; Heterodera glycines, Ichinohe) is an economically damaging pest of soybean in the United States (Allen et al. 2017; Mitchum 2016; Niblack et al. 2006). The SCN has been identified as the disease causing the most yield and dollar loss in soybean in the United States, with annual economic loss from this nematode estimated at more than U.S.$1 billion (Allen et al. 2017; Koenning and Wrather 2010; Wrather and Koenning 2009). This nematode infects soybean but its host range includes other important leguminous crops such as common bean (Phaseolus vulgaris L.) and numerous weed species (Poromarto and Nelson 2009, 2010; Poromarto et al. 2015). The SCN has been detected in all soybean-producing states of the United States (Tylka and Marett 2017). In North Dakota, it was first detected in 2003 in Richland County (Bradley et al. 2004) and, since then, has been detected in at least 19 counties (Yan et al. 2015).
Host resistance and crop rotation are the commonly adopted management practices to control SCN because of their ecofriendly and economical nature (Miller et al. 2006; Niblack et al. 2006; Oyekanmi and Fawole 2010). However, virulence population diversity is becoming a major challenge for managing this nematode. Recent research reports on SCN virulence changes have been published in many soybean-producing states in the United States (Acharya et al. 2016; Niblack et al. 2008; Zheng et al. 2006). Research reports indicate that SCN-resistant cultivars derived from resistance source PI88788 may have reduced effectiveness in controlling H. glycines populations (Acharya et al. 2017; Hershman et al. 2008; McCarville et al. 2017). This situation is mainly due to the continuous planting of the SCN-resistant soybean cultivars derived from a single resistance source, PI 88788. There are a few cultivars derived from Peking and Hartwig but they are not widely used (Mitchum 2016). Although host resistance is the most effective and economical measure for nematode management, it requires a lengthy breeding process and is limited by few available resistance gene sources. To better manage SCN in soybean fields, an alternative integrated approach is necessary. This approach should be able to slow down the virulence changes in SCN population as well as reduce the nematode densities in infested fields. Utilizing cover crops is such an approach for SCN management. Previous research has suggested integrating cover crops into management strategies to help reduce plant-parasitic nematode densities in infested fields (Halbrendt 1996; Kruger et al. 2013). In addition to reduction of nematode numbers, cover crops provide multiple benefits such as improving soil quality for plant growth, improving the nutrient cycle, and preventing soil degradation (Dagel et al. 2014; Hunter et al. 2019; Snapp et al. 2005).
Several different mechanisms appeared to be involved in the reduction of nematode populations by cover crops. An in vitro trial showed greater mortality of the sugar beet cyst nematode (H. schachtii) when treated with the liquid-chromatography fraction derived from marigold seed exudates as compared with the water control (Riga et al. 2005). In Michigan, when oilseed radish (Raphanus sativus L.) was planted before sugar beet (Beta vulgaris L.), the radish acted as a trap crop and reduced the sugar beet cyst nematode population (Poindexter 2011a, b). Many Brassica spp. such as oilseed radish (R. sativus L.), rapeseed (Brassica juncea L.), yellow mustard (Sinapis alba L.), and others have been evaluated for controlling potato cyst nematode in Europe (Lord et al. 2011).
Various research reports have been published on the host plant status of diverse crops and plant species for SCN populations but the effects of cover crops on SCN population reduction (PR) is not well documented. Different crops such as alfalfa (Medicago sativa L.), cabbage (B. oleracea var. capitata L.), cotton, hairy vetch (Vicia villosa L.), red clover, field corn (Zea mays L.), sweet corn (Z. mays L.), tobacco (Nicotiana tabacum L.), and wheat (Triticum aestivum L.) were compared with soybean cultivars for hatching, penetration, and production of mature SCN cysts. Only soybean and hairy vetch supported SCN reproduction, while SCN juveniles barely penetrated red clover and alfalfa (Schmitt and Riggs 1991). A study conducted by Chen et al. (2006) in Minnesota fields showed that interseeding of red clover and alfalfa as cover crops reduced SCN numbers in infested fields. They also suggested that yield reduction of soybean or corn may occur due to competition; therefore, a later planting date for these cover crops may be appropriate for soybean-corn rotation in the northern Great Plains. Three industrial crops—winter camelina (Camelina sativa (L.) Crantz ‘Joelle’), brown mustard (B. juncea L. ‘Kodiak’), and crambe (Crambe abyssinica Hochst. ex R.E.Fr. ‘BelAnn’)—were tested for host and PR of SCN in greenhouse conditions (Acharya et al. 2019). Both winter camelina and brown mustard were nonhosts and reduced the SCN numbers compared with nonplanted natural soil (fallow), while crambe was a poor host and did not reduce SCN numbers consistently compared with the nonplanted control. Root exudates from diverse cover crop species were tested for effects on SCN egg hatching and juveniles. Exudates of annual ryegrass and white clover (Trifolium repens L.) caused significant increases in SCN egg hatching and decreased the number of juveniles by depleting lipid reserves in their body in the absence of host plants (Riga et al. 2001). Furthermore, SCN eggs were able to hatch and penetrate roots of sunn hemp (Crotalaria juncea L.) and showy rattlebox (C. spectabilis L.) but were not able to form mature SCN females and, thus, were unable to continue their life cycle (Kushida et al. 2003).
Several mechanisms may be involved in the interaction of cover crops and SCN. Nonhost status, nematicidal activity of root exudates, and acting as a trap crop may be responsible for reducing nematode numbers when the cover crops or rotation crops are planted in SCN-infested fields (Niblack and Chen 2004; Tylka 2014). However, the effects of cover crops on SCN PR have not been well documented in the northern Great Plains. Therefore, the current research focuses on the potential of utilizing cover crops to enhance sustainable management of H. glycines. Most of the fields in the northern Great Plains remain fallow for about 2 to 3 months after soybean and spring wheat harvesting until covered by snow in the winter. Our goal was to utilize cover crops on those fallow fields. The specific objective of this study was to evaluate the effects of cover crops on PR of SCN populations from North Dakota fields.
Materials and Methods
The cover crops utilized in this study include species from three plant families, including Brassicaceae, Fabaceae, and Poaceae. The crops were selected based on their current or potential use as cover crops in the northern Great Plains (Table 1). A soybean cultivar (Barnes) susceptible to SCN was used as a positive control and a nonplanted treatment was included to represent fallow. Seed were acquired from the Forage and Biomass Crop Production Program at North Dakota State University, Fargo, ND.
H. glycines populations.
Naturally SCN-infested soils were collected from one field each in Cass and Richland Counties in North Dakota. Nematode populations were confirmed as HG type 0 for SCN103 (Richland County) and HG type 7 for SCN2W (Cass County) by using the standard HG typing procedure (Niblack et al. 2002). The soil samples from each field were mixed thoroughly to obtain equal levels of each population in the soil mixtures. The SCN population density of each soil was determined by extracting SCN cysts from three subsamples of 100 cm3 of soil, then crushed to obtain eggs and juveniles and counted under the microscope. For the year 2016, the initial SCN population (eggs and juveniles) per 100 cm3 of soil for each crop was 4,540 and 7,540 for SCN103 and SCN2W, respectively, at the time of planting. For 2017, initial SCN population (eggs and juveniles) per 100 cm3 of soil for each crop was 6,500 and 6,600 for SCN103 and SCN2W, respectively, at the time of planting.
Experiments were conducted in a research field site at North Dakota State University during the second week of August to the first week of November 2016 and repeated once in 2017, with new SCN-infested soil collections in each year. In 2016, the average soil temperature from August to November ranged from 23 to 6°C whereas, in 2017, the average soil temperature from August to November ranged from 21 to 1°C (NDAWN 2019). Microplots were established using large plastic pots (22.86 cm in diameter and 20.30 cm in height) (High Performance 200, Haviland, OH, U.S.A.). Holes were dug in the field plot (dimension of 4.57 by 18.18- m) to hold the plastic pots so that there was about 8 cm of the pot left above the soil surface. The other remaining areas of the field plot area were covered with plastic mesh (weed barrier; ECO gardener premium, 5OZ Pro garden weed barrier landscape fabric) to prevent the growth of weeds and contamination of the pots from surrounding soil. An external fence was built to prevent the entry of animals. Selected crops were planted in each plastic pot containing about 5 kg of soil from each field. Seed were planted equidistantly in each pot at 4 cm from the pot wall. The standard seeding rate of each crop was used for establishing desired plant densities (Midwest Cover Crops Council 2014). After emergence, the plant numbers per pot were adjusted to five plants for carinata and turnip; three plants for annual ryegrass, sweetclover, red clover, foxtail millet, winter rye, and daikon radish; two plants for Austrian winter pea and soybean; and one plant for faba bean. Pots were kept in a greenhouse room for 2 weeks for better plant establishment, then moved to the microplot in the external field environment. The microplot pots were regularly watered to keep required moisture for 2 weeks and fertilized twice with Peter’s 20-10-20 water-soluble complete fertilizer to keep plants growing. Seventy-five days after pots were placed in the field, three soil cores were collected from each pot through the vegetation by taking soil across the rhizosphere area of the plants, and three random soil cores were also collected from the fallow pots without plants. These three cores were thoroughly mixed; then, a subsample of 100 cm3 of soil was used to determine the final population density (FPD) (eggs and juveniles). First, SCN cysts were extracted by pouring soil and water suspension from a 4-liter bucket filled three-quarters full of water into a 250-µm-pore sieve nested under a 710-µm-pore sieve using a standard method described previously (Krusberg et al. 1994). The extracted cysts were crushed by a rubber stopper attached to a motorized drill press (MasterForce Drill Press, Menards, Fargo, ND, U.S.A.) to release the eggs and juveniles, as described by Faghihi and Ferris (2000). The resultant SCN eggs and juveniles were counted under the microscope (Zeiss Axiovert 25; Carl Zeiss Microscopy, White Plains, NY, U.S.A.) to determine the final SCN population density for each crop, including nonplanted natural soil. The percent population suppression by each of the tested crops was calculated by comparing FPD in the crop and FPD in fallow to evaluate the effect on SCN populations by each crop but not from natural mortality in nonplanted natural soil by using the following formula:
Moreover, the percent PR of each cover crop, including the nonplanted natural soil, was calculated by comparing with their initial population density to ascertain the dynamic population change over time by using following formula:
The ability of cover crops to reduce SCN population was compared with the nonplanted naturally infested soils for both SCN populations.
The experimental design for the microplot experiments was a randomized complete block design with five replications. Data for each year were analyzed using SAS 9.4 (SAS Institute, Cary, NC, U.S.A.) separately, because the initial SCN population in each of the experiments was different. The analysis of variance was performed by using the general linear model with Tukey’s honestly significant difference mean separation at the significance level of 5% to determine the significant difference in final SCN populations and average PR among the treatments and controls.
Final SCN population density.
In 2016, SCN103 had significantly (P < 0.0001) lower average FPD (1,262 to 2,996 eggs and juveniles/100 cm3 of soil) on all tested crops except Austrian winter pea, faba bean, and foxtail millet, compared with susceptible soybean Barnes (FPD: 4,113) (Table 2). SCN2W had significantly (P < 0.0001) lower average FPD (2,398 to 5,474) on all tested cover crops compared with susceptible soybean Barnes (11,250). For the SCN2W population, the average FPD on Australian winter pea and nonplanted natural soil were significantly greater than all other tested cover crops, except faba bean and carinata, but significantly lower than susceptible soybean Barnes (Table 2).
In the 2017 microplot experiments, SCN103 had significantly (P < 0.0001) lower average FPD (1,820 to 3,620) on all tested crops compared with the nonplanted control, Austrian winter pea, and susceptible soybean Barnes (FPD = 6,180, 6,620, and 26,960, respectively). The average FPD on Austrian winter pea and nonplanted natural soil were greater than in all other crops but significantly lower than susceptible soybean Barnes (Table 3). SCN2W had significantly (P < 0.0001) lower average FPD (2,800 to 6,720) on all tested cover crops and nonplanted natural soil compared with susceptible soybean Barnes (21,180). None of the cover crops had a significantly greater average FPD than the nonplanted soil (Table 3). A significant difference (P < 0.0001) was observed in the percent population suppressions by some cover crops and by the nonplanted natural soil. All of the crops, except Austrian winter pea and susceptible soybean Barnes suppressed SCN numbers by 25 to 72% of the fallow in 2016 and by 32 to 70% of the fallow in 2017 for the two SCN populations (SCN103 and SCN2W). Susceptible soybean Barnes either almost maintained or increased (up to 341%) SCN numbers, and the Austrian winter pea either maintained or increased the SCN numbers up to 11% of the fallow for both SCN populations for both years (Tables 2 and 3).
PR of SCN.
When compared with initial population densities, significant differences (P < 0.0001) were observed in the PR by cover crops and natural reduction in nonplanted natural soil in microplot experiments in both 2016 and 2017. In 2016, all of the tested cover crops, except Austrian winter pea and faba bean, reduced the SCN103 numbers compared with the initial population density and the reduction was significantly (P < 0.0001) greater (PR = 33 to 73%) than in nonplanted natural soil (PR = 1%). The greatest reduction in SCN density was caused by annual ryegrass (72%), followed by daikon radish (70%), turnip (62%), carinata (56%), and 46 to 34% by red clover, winter rye, and foxtail millet (Fig. 1). For SCN2W, all of the cover crops except Austrian winter pea, carinata, and faba bean significantly reduced SCN numbers based on the initial population density and the reduction was significantly (P < 0.0001) greater (PR = 53 to 68%) than in nonplanted natural soil (PR = 24%). The greatest reduction in SCN density was caused by daikon radish (68%), followed by annual ryegrass (67%), foxtail millet (64%), sweetclover (62%), turnip (60%), and 53 to 57% by red clover and winter rye (Fig. 1). The PR by Austrian winter pea was only 1% for SCN103 and 28% for SCN2W, which were not significantly different than the nonplanted control.
In 2017, all of the tested crops except Austrian winter pea reduced SCN103 numbers compared with the initial population density and the reduction was significantly (P < 0.0001) greater (PR = 44 to 72%) than in nonplanted natural soil (PR = 5%) (Fig. 2). Daikon radish resulted in the greatest PR of 71%, followed by 68% by annual ryegrass, 57% by carinata, 55% by foxtail millet, and 50 to 44% by faba bean, turnip, red clover, winter rye, and sweetclover (Fig. 2). For SCN2W, all of the tested crops except Austrian winter pea and foxtail millet reduced SCN numbers compared with the initial population density and the reduction was significantly (P < 0.0001) greater (PR = 41 to 58%) than in nonplanted natural soil (PR = 4%). The greatest PR (58%) was by turnip, then 56% by daikon radish, 54% by annual ryegrass, and 52 to 45% by faba bean, winter rye, sweetclover, red clover, and carinata (Fig. 2). Austrian winter pea increased the SCN103 and SCN2W populations by about 1%. The greatest PR was observed in the infested soil planted with annual ryegrass and daikon radish, with an average PR of 65 and 67% compared with initial numbers, respectively, averaged over both populations and both years.
All of the tested cover crops and nonplanted natural soil except Austrian winter pea, faba bean, and foxtail millet for SCN103 in 2016 had significantly lower FPD compared with susceptible soybean in both years when tested in microplot experiments conducted in SCN-infested soils from two fields in North Dakota. The majority of the tested crops were nonhosts for both SCN populations, except Austrian winter pea and turnip, which were poor hosts for SCN (Acharya et al. 2020). The host status for SCN was determined based on the number of white females produced on a crop with respect to susceptible soybean and expressed in percentage as a female index (FI), where the crop with FI = 0 is considered as nonhost, FI > 0 < 10 as poor host, and FI ≥ 10 as suitable host (Niblack et al. 2002; Poromarto and Nelson 2010). The percent population suppression based on FPD of the crop compared with FPD in fallow suggested that all of the crops suppressed SCN population increase, except Austrian winter pea and susceptible soybean. This population suppression calculation method based on the fallow treatment was intended to discern the effect on SCN populations directly from each crop but not from natural kill in the nonplanted natural soil. Overall, from 2 years of experiments, Austrian winter pea almost maintained SCN populations, and susceptible soybean significantly increased the SCN numbers. The soybean was included as a susceptible check but variability was observed in the final SCN populations between the 2 years of the experiments. This variability may be due to the planting date in August and less plant growth before winter-kill compared with normal soybean growth in the normal growing season. Environmental factors such as soil moisture and temperature might have played a role, although we could not detect good correlations when we looked at the weather data.
The percent PR of each cover crop suggested that all of the cover crops tested except Austrian winter pea, faba bean, carinata, and foxtail millet had significantly greater percent PR than in the nonplanted natural soil in both years’ experiments. This PR calculation method based on the initial population density was intended to observe the dynamic population change over time for each crop. This would also provide information for growers when they may not include the fallow treatment in their infested fields and are not able to compare the effect of cover crops with the fallow. Overall, the crops that were effective in reducing the SCN populations were nonhosts, which supports the concept that nonhost crop rotation is one of the important strategies for SCN management (Chen et al. 2001; Hunter et al. 2019; Warnke et al. 2006). Consistent responses were observed in the PR of SCN by annual ryegrass, daikon radish, red clover, sweetclover, turnip, and winter rye in microplot experiments. However, results for carinata, faba bean, and foxtail millet for reducing SCN numbers were inconsistent, even though they were effective in reducing SCN densities in infested soil for at least one of the SCN populations or in 1 year of the experiments.
Our results confirm the findings from the previous study conducted by Chen et al. (2008), where they found that red clover was effective in reducing SCN number in infested soils. For Brassica spp., daikon radish, turnip, and carinata significantly reduced SCN populations in both years of the microplot studies, except carinata for SCN2W in 2016. Our results support the results from previous studies, where many Brassica spp. such as yellow mustard, rapeseed, oilseed radish, and others were able to reduce potato cyst nematode (Lord et al. 2011; Ngala et al. 2015). These reports support the idea that brassicas can play an important role in SCN management if included in an integrated pest management scheme (Avato et al. 2013; Dutta et al. 2019). Annual ryegrass, foxtail millet, and winter rye from the Poaceae family consistently reduced the initial SCN populations compared with fallow for both SCN populations except foxtail millet, which did not significantly reduce SCN2W in an experiment in 2017 (Fig. 2). Our results showing that annual ryegrass reduces the SCN population when planted in SCN-infested soils confirms previous research by Pedersen and Rodriguez-Kabana (1991) and Riga et al. (2001). To our knowledge, no published reports are available for foxtail millet and winter rye regarding SCN PR when planted in infested soils.
Although mechanisms of PR by cover crops are still unclear, some previous experiments have attempted tested root exudates from different cover crops of different plant families (Kushida et al. 2003; Riga et al. 2001). Induced SCN egg hatching, nematicidal activity, and trap crops were proposed to be mechanisms of SCN PR by cover crops (Kushida et al. 2003; Riga et al. 2001; Tylka 2014; Warnke et al. 2006). It is possible that these mechanisms may have played a role in PR of SCN populations in this study, where we had diverse cover crops species from three different plant families (Brassicaceae, Fabaceae, and Poaceae). Further studies such as analysis of root exudates, penetration of juveniles, subsequent development of SCN, and visualization for nematodes inside the root tissue in these crops will be required to confirm the mechanisms of PR. Populations of both SCN103 and SCN2W were considerably reduced in the nonplanted natural soil. The juveniles hatched in nonplanted soils eventually die by not getting a host to infect and feed upon. It is also obvious that hatching of SCN eggs is influenced by temperature and other environmental conditions (Tefft et al. 1982).
This study shows that some cover crops can reduce SCN population densities when planted in infested soils. Our results are similar to other studies, which found that cover crops were able to reduce population densities of H. glycines and H. schachtii in microplot and field conditions (Riga et al. 2001, 2005). Although the results from field and greenhouse studies on interaction between SCN and covers crops were inconsistent, fewer SCN white females were recovered in some cover crops treatments such as annual ryegrass, crimson clover, daikon radish, and their crop mix compared with the nonplanted control when followed by soybean in a greenhouse experiment (Harbach 2019). In this study, annual ryegrass, daikon radish, and turnip consistently reduced SCN populations by more than 50% in both years, suggesting that cover crops from the families Poaceae and Brassicaceae have potential use in northern Great Plains soybean growing systems.
Most of the selected crops in our study are winter cover crops, which can be planted after soybean or wheat harvesting to provide cover to fallow land before the winter-kill. Planting these cover crops after soybean or spring wheat harvesting might be more appropriate than planting them as interseeded crops, because the cover crops may compete with the main crop and reduce the yields (Chen et al. 2006). Although these crops reduced SCN numbers and have potential to be planted after soybean and spring wheat harvesting, not all will produce as much biomass as in the normal growing season. For example, foxtail millet is a summer cover crop and requires relatively high temperatures for optimum growth (Doust et al. 2009). Therefore, further evaluation in the normal growing season might be helpful to understand its effects on SCN population dynamics. Miller et al. (2006) suggested that nonhost and poor host leguminous crops may reduce SCN numbers in infested fields but planting in a single season may not result in significant reductions if susceptible soybean was planted after those crops. In addition to the SCN PR, these crops may add value by improving soil properties (Cai et al. 2019). Further studies such as determining mechanisms of PR and economic and agronomical benefits of cover crops should be performed to understand the applicability of these crops in an integrated SCN management strategy.
We thank I. Choudhury and A. KC for their help with this project by preparing microplot and soil sampling, M. Berti for providing cover crop seed for this study, and the growers who allowed us to collect soil samples from their fields.
The author(s) declare no conflict of interest.
- 2016. Determination of Heterodera glycines virulence phenotypes occurring in South Dakota. Plant Dis. 100:2281-2286. https://doi.org/10.1094/PDIS-04-16-0572-RE Link, ISI, Google Scholar
- 2017. Assessment of commercial soybean cultivars for resistance against prevalent Heterodera glycines populations of South Dakota. Plant Health Prog. 18:156-161. https://doi.org/10.1094/PHP-03-17-0017-RS Link, ISI, Google Scholar
- 2019. Can winter camelina, crambe, and brown mustard reduce soybean cyst nematode populations? Ind. Crops Prod. 140:111637. https://doi.org/10.1016/j.indcrop.2019.111637 Crossref, ISI, Google Scholar
- 2020. Evaluation of diverse cover crops as hosts of two populations of soybean cyst nematode, Heterodera glycines. Crop Prot. 135:105205. doi:10.1016/j.cropro.2020.105205 Crossref, ISI, Google Scholar
- 2017. Soybean yield loss estimates due to diseases in the United States and Ontario, Canada from 2010 to 2014. Plant Health Prog. 18:19-27. https://doi.org/10.1094/PHP-RS-16-0066 Link, ISI, Google Scholar
- 2013. Nematicidal potential of Brassicaceae. Phytochem. Rev. 12:791-802. https://doi.org/10.1007/s11101-013-9303-7 Crossref, ISI, Google Scholar
- 2004. First report of soybean cyst nematode (Heterodera glycines) on soybean in North Dakota. Plant Dis. 88:1287. https://doi.org/10.1094/PDIS.2004.88.11.1287A Link, ISI, Google Scholar
- 2019. Economic impacts of cover crops for a Missouri wheat–corn–soybean rotation. Agriculture 9:83 https://www.mdpi.com/2077-0472/9/4/83. https://doi.org/10.3390/agriculture9040083 Crossref, Google Scholar
- 2008. Effect of rotation crops on hatch, viability and development of Heterodera glycines. Nematology 10:869-882. https://doi.org/10.1163/156854108786161391 Crossref, ISI, Google Scholar
- 2001. Crop sequence effects on soybean cyst nematode and soybean and corn yields. Crop Sci. 41:1843-1849. https://doi.org/10.2135/cropsci2001.1843 Crossref, ISI, Google Scholar
- 2006. Effect of cover crops alfalfa, red clover, perennial ryegrass, and rye on soybean cyst nematode population and soybean and corn yields in Minnesota. J. Nematol. 38:267. ISI, Google Scholar
- 2014. Improving soybean performance in the northern Great Plains through the use of cover crops. Commun. Soil Sci. Plant Anal. 45:1369-1384. https://doi.org/10.1080/00103624.2014.884108 Crossref, ISI, Google Scholar
- 2009. Foxtail millet: A sequence-driven grass model system. Plant Physiol. 149:137-141. https://doi.org/10.1104/pp.108.129627 Crossref, ISI, Google Scholar
- 2019. Plant-parasitic nematode management via biofumigation using brassica and non-brassica plants: Current status and future prospects. Curr. Plant Biol. 17:17-32. https://doi.org/10.1016/j.cpb.2019.02.001 Crossref, ISI, Google Scholar
- 2000. An efficient new device to release eggs from Heterodera glycines. J. Nematol. 32:411-413. ISI, Google Scholar
- 1996. Allelopathy in the management of plant-parasitic nematodes. J. Nematol. 28:8-14. ISI, Google Scholar
- 2019. Investigating the interactions between cover crops and the soybean cyst nematode through lab, greenhouse, and field studies. Ph.D. dissertation 17459, Iowa State University. https://lib.dr.iastate.edu/etd/17459 Google Scholar
- 2008. Soybean cyst nematode, Heterodera glycines populations adapting to resistant soybean cultivars in Kentucky. Plant Dis. 92:1475. https://doi.org/10.1094/PDIS-92-10-1475B Link, ISI, Google Scholar
- 2019. Cover crop mixture effects on maize, soybean, and wheat yield in rotation. Agric. Environ. Lett. 4:180051. https://doi.org/10.2134/ael2018.10.0051 Crossref, ISI, Google Scholar
- 2010. Suppression of soybean yield potential in the continental United States by plant diseases from 2006 to 2009. Plant Health Prog. 11. doi.org/10.1094/PHP-2010-1122-01-RS Link, Google Scholar
- 2013. Cover crops with biofumigation properties for the suppression of plant-parasitic nematodes: A review. S. Afr. J. Enol. Vitic. 34:287-295. ISI, Google Scholar
- 1994. A method for recovery and counting of nematode cysts. J. Nematol. 26:599. ISI, Google Scholar
- 2003. Effects of Crotalaria juncea and C. spectabilis on hatching and population density of the soybean cyst nematode, Heterodera glycines (Tylenchida: Heteroderidae). Appl. Entomol. Zool. 38:393-399. https://doi.org/10.1303/aez.2003.393 Crossref, ISI, Google Scholar
- 2011. Biofumigation for control of pale potato cyst nematodes: Activity of brassica leaf extracts and green manures on Globodera pallida in vitro and in soil. J. Agric. Food Chem. 59:7882-7890. https://doi.org/10.1021/jf200925k Crossref, ISI, Google Scholar
- 2017. Increase in soybean cyst nematode virulence and reproduction on resistant soybean varieties in Iowa from 2001 to 2015 and the effects on soybean yields. Plant Health Prog. 18:146-155. https://doi.org/10.1094/PHP-RS-16-0062 Link, ISI, Google Scholar
Midwest Cover Crops Council. 2014. Midwest Cover Crops Field Guide, 2nd ed. Purdue Extension Publication. Purdue University, West Lafayette, IN, U.S.A. Google Scholar
- 2006. Rotation crop evaluation for management of the soybean cyst nematode in Minnesota. J. Agron. 98:569-578. https://doi.org/10.2134/agronj2005.0185 Crossref, ISI, Google Scholar
- 2016. Soybean resistance to the soybean cyst nematode Heterodera glycines: An update. Phytopathology 106:1444-1450. https://doi.org/10.1094/PHYTO-06-16-0227-RVW Link, ISI, Google Scholar
NDAWN. 2019. North Dakota Agricultural Weather Network: Mooreton, ND station. https://ndawn.ndsu.nodak.edu/station-info.html?station=54 Google Scholar
- 2015. Biofumigation with Brassica juncea, Raphanus sativus and Eruca sativa for the management of field populations of the potato cyst nematode, Globodera pallida. Pest Manage. Sci. 71:759-769. https://doi.org/10.1002/ps.3849 Crossref, ISI, Google Scholar
- 2002. A revised classification scheme for genetically diverse populations of Heterodera glycines. J. Nematol. 34:279-288. ISI, Google Scholar
- 2006. A model plant pathogen from the kingdom animalia: Heterodera glycines, the soybean cyst nematode. Annu. Rev. Phytopathol. 44:283-303. https://doi.org/10.1146/annurev.phyto.43.040204.140218 Crossref, ISI, Google Scholar
- 2004. Cropping systems. Pages 181-206 in: Biology and Management of the Soybean Cyst Nematode, 2nd ed. D. P. Schmitt, J. A. Wrather, and R. D. Riggs, eds. Schmitt and Assoc., Marceline, MO, U.S.A. Google Scholar
- 2008. Shift in virulence of soybean cyst nematode is associated with use of resistance from PI 88788. Plant Health Prog. 9. doi.org/10.1094/PHP-2008-0118-01-RS Link, Google Scholar
- 2010. Nematodes of soybean and their management. Pages 325-344 in: The Soybean: Botany, Production and Uses. G. Singh, ed. CABI, Rawalpindi, Pakistan. https://doi.org/10.1079/9781845936440.0325 Crossref, Google Scholar
- 1991. Winter grass cover crop effects on nematodes and yields of double cropped soybean. Plant Soil 131:287-291. https://doi.org/10.1007/BF00009460 Crossref, ISI, Google Scholar
- 2011a. Managing sugar beet cyst nematode. Michigan State University Extension. https://www.canr.msu.edu/news/managing_sugar_beet_cyst_nematode Google Scholar
- 2011b. Oilseed radish cover crops in sugarbeet rotations improves nematode control. Michigan State University Extension. https://www.canr.msu.edu/news/oilseed_radish_cover_crops_in_sugarbeet_rotations_improves_nematode_control Google Scholar
- 2015. Evaluation of weed species from the northern Great Plains as hosts of soybean cyst nematode. Plant Health Prog. 16:23-28. https://doi.org/10.1094/PHP-RS-14-0024 Link, Google Scholar
- 2009. Reproduction of soybean cyst nematode on dry bean cultivars adapted to North Dakota and northern Minnesota. Plant Dis. 93:507-511. https://doi.org/10.1094/PDIS-93-5-0507 Link, ISI, Google Scholar
- 2010. Evaluation of northern-grown crops as hosts of soybean cyst nematode. Plant Health Prog. 11. doi.org/10.1094/PHP-2010-0315-02-RS Link, Google Scholar
- 2005. In vitro effect of marigold seed exudates on plant parasitic nematodes. Phytoprotection 86:31-35. https://doi.org/10.7202/011712ar Crossref, ISI, Google Scholar
- 2001. The impact of plant residues on the soybean cyst nematode, Heterodera glycines. Can. J. Plant Pathol. 23:168-173. https://doi.org/10.1080/07060660109506926 Crossref, ISI, Google Scholar
- 1991. Influence of selected plant species on hatching of eggs and development of juveniles of Heterodera glycines. J. Nematol. 23:1-6. ISI, Google Scholar
- 2005. Evaluating cover crops for benefits, costs and performance within cropping system niches. J. Agron. 97:322-332. Crossref, ISI, Google Scholar
- 1982. Factors influencing egg hatching of the soybean cyst nematode. Proc. Helminthol. Soc. Wash. 49:258-265. Google Scholar
- 2014. Cover crops and SCN: What’s the connection? Iowa State University, Extension and Outreach. https://crops.extension.iastate.edu/cropnews/2014/09/cover-crops-and-scn-whats-connection Google Scholar
- 2017. Known distribution of the soybean cyst nematode, Heterodera glycines, in the United States and Canada, 1954 to 2017. Plant Health Prog. 18:167-168. https://doi.org/10.1094/PHP-05-17-0031-BR Link, ISI, Google Scholar
- 2006. Effect of rotation crops on Heterodera glycines population density in a greenhouse screening study. J. Nematol. 38:391-398. ISI, Google Scholar
- 2009. Effects of diseases on soybean yields in the United States 1996 to 2007. Online. Plant Health Prog. 10:24. https://doi.org/10.1094/PHP-2009-0401-01-RS Link, Google Scholar
- 2015. The status of soybean cyst nematode occurrence and management in North Dakota. Pages 126-127 in Abstr. 54th Annu. Meet. Soc. Nematol. Google Scholar
- 2006. Characterization of the virulence phenotypes of Heterodera glycines in Minnesota. J. Nematol. 38:383-390. ISI, Google Scholar
The author(s) declare no conflict of interest.
Funding: We thank the North Dakota Soybean Research Council for funding this research.