NE1640: Plant-Parasitic Nematode Management as a Component of Sustainable Soil Health Programs in Horticultural and Field Crop Production Systems

(Multistate Research Project)

Status: Inactive/Terminating

NE1640: Plant-Parasitic Nematode Management as a Component of Sustainable Soil Health Programs in Horticultural and Field Crop Production Systems

Duration: 10/01/2016 to 10/01/2021

Administrative Advisor(s):


NIFA Reps:


Non-Technical Summary

Statement of Issues and Justification

Statement of Issues and Justification:


The need. The Northeast Region has a great diversity of economically significant plants that are susceptible to yield and quality damage caused by a broad array of plant-pathogenic nematodes. In addition, bacterial- and fungal-feeding nematodes are important organisms for nutrient cycling, essential for plant growth and development. There are, however, very few nematologists in the Region with formal Extension or other outreach responsibilities. For the research results associated with this project to be adopted by crop/plant producers, agribusiness professionals, government agency policy and Extension educators, it is imperative for the project to have a strong, dynamic and modern system of education, facilitation and persuasion designed to enhance the socio-economic and environmental future of agriculture, ornamental and recreational sectors of the region.


Root-knot, lesion and dagger nematodes are important plant-parasites and pathogens that continue to cause substantial crop suppression and losses on important agronomic and horticultural crops grown in the northeastern United States. These soilborne plant pathogens frequently require implementation of varying management practices, often on an annual basis. Soil applications of chemical nematicides continue to be used as the primary method for nematode management, especially on high value vegetable and fruit crops, however, they may not be available or practical for a number of crops. Members of NE-1040 have made significant progress in identifying alternative nematode management options for fruits such as apples, peaches, strawberries, and vegetables including beans, carrots, onions, peppers, potatoes, tomatoes, and others, based on using nematode suppressive cover and rotational crops, biofumigants, resistant cultivars, and effective biological control agents, such as Pasteuria penetrans and P. thornei. In addition, the group has made progress in assessing the impact of selected cultural production practices on the diversity of nematode community structure at the trophic level and the nature of nematode communities. This research approach requires significant additional research and integration into overall sustainable soil health management programs.


Intensive production of agronomic and horticultural crops in the northeastern region has resulted in a gradual deterioration of soil quality contributing to reduced yield and profitability. The method of ‘intensifying’ agricultural production is a matter of debate. Since the Green Revolution, the focus has been on intensive use of inputs (seeds, fertilizers, and pesticides) to maximize productivity.  This approach has had negative impacts on human health and the environment (Chappell and Lavalle, 2011; Bommarco et al.,2013). What we are proposing is ecological or sustainable intensification where agricultural systems are managed to increase productivity without adverse environmental impact and without conversion of additional non-agricultural land (Pretty and Bharucha 2014). Production of food, environment and human health are interdependent and not mutually exclusive.  It has also become obvious that increasing inputs and the intensity of production practices, such as tillage, are no longer effective in attaining and maintaining profitable crop yields.  Causes of poor soil quality include: soil compaction, crusting, low organic matter content, increased pressure from soilborne plant pathogens, insects and weeds, and lower density and diversity of soil food-web organisms (often referred to as beneficial soil organisms).  Growers, extension educators and researchers now realize the need for the implementation of practical and sustainable soil management programs to improve soil productivity and farm profitability.  These concepts of soil health and biologically based agriculture involve the integration and optimization of soil physical, chemical and also biological factors for improved soil function (productivity) in an economically and environmentally compatible manner.  Several multi-disciplinary soil health teams in the United States and abroad have been established to address soil health degradation issues and to develop holistic and long-term sustainable solutions.  Significant progress has been made to date, including the development of cost-effective protocols for assessing the status of soil health, increasing soil health literacy, facilitating soil health demonstrations by growers, and promoting multi-disciplinary research and outreach.  Although nematodes have been used as comprehensive biological models for all of science and nematodes have recently been utilized as important biological indicators of soil health, comparatively little is known about the relationships between soil health and management of plant-pathogenic nematodes. There is an immediate need to assess the impact of soil health interventions, and the use of biological control organisms and plant resistance on nematode community structure dynamics.  Further, research is required to integrate nematode management recommendations into soil health management programs designed for specific agronomic and horticultural production systems.  The expansion of the soil health and biological components of this project are, in part, in response to suggestions made by the Northeast Directors in their review of the previous multistate project.  Thus, we propose to address these needs in a new, five-year multistate project with a focus on developing biologically based nematode management practices that are not only compatible with overall soil health management practices, but are designed as integral components of these systems.


Stakeholder priorities that emphasize the need for this research identified through the National IPM Road Map and Northeast IPM priorities include: increased emphasis on bio-based pest management; developing alternative (non-chemical) pest management systems; the synergism of IPM programs with organic or biological control programs; the development of new generation low-risk suppression tactics including biological control and products of traditional breeding and biotechnology; as well as the creation and dissemination of educational guidelines for use of biological and cultural mgmt tactics.


Importance of work and consequences if not done. United States consumers demand high quality, readily available and inexpensive food and fiber. For this to be achieved by northeastern producers of agronomic and horticultural crops, it is imperative that sustainable soil health systems be maintained, or in some cases, restored. Nematodes play three critical roles in this challenge: (i) the occurrence of high population densities of plant-pathogenic nematodes results in low yields of poor quality produce, makes farming less profitable and is a key component of poor quality soil; (ii) bacterial- and fungal-feeding nematodes are key components of soil food webs and are essential for optimal plant nutrition; and (iii) nematode community structure assessment has become recognized as an important tool for measuring soil quality. Northeastern farmers are very interested in management of plant-pathogenic nematodes, the sustainability of soil health, soil quality restoration and having significantly improved nematode and soil management tools. Modern science recognizes nematodes as the most prominent group of animals on our planet. An understanding of the role of nematodes in how northeastern ecosystems work is essential for appropriate decision-making in regards to the overall environmental health and human quality of life for the region. The Regional Research System forms the foundation for nematologists from academia and USDA to work together on common research and education initiatives of significance to the region. Neither the private sector nor government has the nematology resources to fulfill this critical need.


Technical feasibility of work. The following three items strongly defend the feasibility of the proposed work: 1) Milestones in the current project have been consistently met and the proposed project builds on this previous work. The progress made by the researchers associated with the current NE-1040 Multistate Research Project is a strong indication that plant-pathogenic nematodes can be managed in a reliable manner with cultural management tactics based on host resistance, nematode antagonistic rotation or cover crops, soil amendments, and biological agents, 2) the roles of bacterial-and fungal-feeding nematodes in plant nutrition have been validated in several laboratories and technology has been developed for the use of nematode community structure assessment for analysis of soil quality, and 3) several members of the NE-1040 currently work closely with sustainable soil health management teams and have been involved with grower education, train-the trainer programs and agribusiness workshops. Currently the biggest challenge for Objective 3 is to identify a coordinator for the last four years of the project, a high quality webmaster and an appropriate site for the server. Professor Bird of Michigan has agreed to coordinate Objective 3 for 2017. Both University of Florida and Michigan State University are in the process of filling Applied Nematology-Extension positions. URI is slated to hire a Soil Health biologist in 2017. Objective 3. of the NE Regional Nematology Research Project should be an ideal 2018-2021 leadership focal point for one or more of these individuals.


Advantages of a multistate effort. The diverse and complex nature of Northeastern agriculture and its associated poly-specific nematode communities offer challenges that are correspondingly diverse and complex. Nematology, however, is only represented by a very small number of scientists, especially in the Northeast. To achieve the objectives of this project, it is imperative that these individuals have the opportunity to work together as team members of a multistate research project. With current limited nematology personnel and resources, it would not be possible to achieve the objectives of this proposed project if pursued on an individual agricultural experiment station basis. For example, NE-1040 is currently sponsoring a Nematology short course for agri-business that addresses the role of nematodes in crop losses and nematode management with rotation and cover crops as well as breeding plants for resistance to nematodes. No one scientist could develop or present such a program. In addition, interaction through the multistate project has led to a number of grant proposals and successful projects by project participants that leverage addition support dollars for needed research.


The NE regional nematology project forms a strong multistate foundation for nematologists from academia and USDA to work together on common research and education initiatives of significance to the overall well-being of the region. Private sector enterprises and government agencies do not have the nematology resources and institutional structures necessary to fulfill this critical need in a satisfactory manner. The NE regional nematology research project has provided nematology leadership for the region since its inception in 1954.


Impacts of work. The proposed multistate research project will: 1) enhance the economic viability of farms by saving costs associated with nematicide usage and 2) change the behaviors of farmers through extension and outreach to result in increased integrated management of nematodes, thereby increasing sustainable soil health of small, medium and large farms throughout the northeastern region. In addition, farmers will have an increased overall understanding about the nature of nematodes, the damage they can cause, and the key roles that these animals have in soil food webs. There will also be significant new knowledge added to the science of nematology.

Related, Current and Previous Work

There are currently three other multistate research projects that focus on plant-pathogenic nematodes: S1066, NC1197, and W3186. These multistate projects differ in regards to the cropping systems, the nematode species investigated, and the research approaches utilized. S1066 has three main objectives, the first being tools for identification of nematode species and characterization of intraspecific variability, the second examining molecular and physiological mechanisms of plant-nematode interactions and the third integrating management tactics into sustainable systems. The southern project has primary interest on cotton, peanut, corn, and soybean, and its focus on host resistance in one or more of these crops to the southern root-knot nematode M. incognita, the reniform nematode Rotylenchulus reniformis, and the soybean cyst nematode Heterodera glycines. NC1197 focuses primarily on nematode management for soybean and corn as major crops in the north-central US. W3186 investigates variability and adaptation of plant-pathogenic nematode populations, as well as management, for a wide variety of nematode parasites in relation to impacts on crop production and trade in the western US. The nematodes of concern include several southern root-knot nematode species, temperate root-knot including M chitwoodi and M. hapla, and multiple cyst nematode species, including potato cyst nematodes with restricted trade or quarantine status. Our project has some overlap with the southern multistate effort dealing with host resistance (S1066), inasmuch as both include biological management, rotation and plant resistance for nematode management, but the crops and target nematodes have relatively little overlap.


The loss of multi-purpose soil fumigants, such as methyl bromide, as well as several traditional nematicides from the market due to environmental concerns and the costs of re-registration has focused attention on the development of host resistance, nematode antagonistic rotation or cover crops, soil amendments and biological agents (Hirunslee et al., 1995; McSorley and Dickson, 1995; McSorley and Gallaher, 1992; Rodriguez-Kabana and Kloepper, 1998; Weaver et al., 1995).  The development and deployment of plant resistance to nematodes may be the single most effective means of managing these plant-parasites.  Fumigant nematicides have ‘sterilized’ the soil and given favor to pathogens to have a competitive advantage in recolonizing over the beneficials. This may be analogous to the gut microbiome and how the whole suite of beneficial microbes is important for a well-functioning and healthy agricultural ecosystem (Chaparro et al., 2012).  Conversely, harnessing the beneficial biology in soils requires a different approach. It is more knowledge intensive.  We have to understand the ecology of the beneficial organisms so they are given a competitive advantage over the pathogen (Philippot et al., 2013).  Plant resistance limits reproduction of the nematodes in the target crop and in some cases can be as effective as chemical control (Cook and Evans, 1987; Starr and Roberts, 2004).  In one study of the economic benefits, the $1 million cost of developing a soybean cultivar resistant to cyst nematodes was far surpassed by $400 million in benefit (Brady and Duffy, 1982).  Most resistance has been investigated against root-knot and cyst nematodes, and that will be the primary thrust in these efforts.  Deployment strategies for utilizing resistance will also be investigated.  RKN resistant vegetable cultivars as rotational crops may limit damage in subsequently planted susceptible crops.  Cucumber and muskmelons double-cropped after a RKN resistant tomato produced increased yield, had reduced root-galling, and lower densities of M. incognita second-stage juveniles (J2) in soil than the same cucumber and muskmelon cultivars grown after a susceptible tomato (Colyer et al., 1998; Hannah et al., 1994; Hannah, 2000).  The RKN resistant pepper Carolina Cayenne was effective as a rotation crop for managing M. incognita in susceptible bell peppers (Thies et al., 1998).  Yield of squash grown in the spring following a rotation crop of castor, cotton, velvetbean, or crotalaria, produced heavier yields than squash grown after RKN susceptible peanut (McSorley et al., 1994).  When eggplant was grown following resistant ‘Mississippi Silver’ southernpea, root galling by M. incognita race 1 was less severe than when eggplant was grown following susceptible ‘Clemson Spineless’ okra (McSorley and Dickson, 1995).  While the above studies demonstrate the concept and utility of plant resistance, most resistance genes are not effective against northern root-knot nematodes, requiring unique screening efforts and research.


Crop rotation is a beneficial production practice and has been extensively studied as a more sustainable nematode and pathogen management measure than chemical pesticides. Crop rotations often reduce nematode populations by reducing reproductive potential and survival, eliminating or reducing population densities.  Crop rotations and cover crops also can lead to disease reduction by increasing the abundance or activity of beneficial soil microflora.  In such cases, the crop used in the rotation sequence is often selected for the development of a beneficial rhizosphere microbial community (Kloepper et al., 1991; Latour et al., 1996; Smith and Goodman, 1999; Weller et al., 2002).  Among the organisms that are most likely favored by cover crops are fungal egg-parasites, nematode-trapping fungi, endoparasitic fungi, endomycorrhizal fungi, plant-health promoting rhizobacteria, and obligate bacterial parasites (Sikora, 1992).  The use of legume cover or rotation crops provides organic nitrogen while also suppressing plant-parasitic nematodes.  Unfortunately, many legumes are susceptible to RKN (Meloidogyne spp.), which is often the key nematode pathogens requiring management in many cropping systems (McSorley, 1998, 1999).  A number of legume crops have been identified that are highly resistant to various species and/or races of RKN.  Some of these, cowpea (Vigna unguiculata), velvetbean (Mucuna deeringiana), and sunn hemp (Crotalaria juncea) have potential in cropping systems (McSorley, 1999; Rodriguez-Kabana, et al., 1988, 1989; Sipes and Arakaki, 1997; Weaver et al., 1995).  In addition to nematode management and nitrogen provided by nematode-resistant legumes, crop residues may increase levels of soil organic matter, improving water-holding capacity and other soil properties (McSorley and Gallaher, 1995).


Crop rotations can reduce certain nematode densities, but may actually increase populations of other nematode pathogens (LaMondia and Halbrendt, 2003; Noe, 1998). Growers must consider multiple factors including economic returns of rotation crops, additional capital and labor requirements, and grower and market acceptance of the rotation crop. Although crop rotation itself is unlikely to provide nematode management in all crop systems, when integrated with other non-chemical management measures such as biological control, rotation is likely to become increasingly important, as synthetic nematicide options are lost. Several nematode-antagonistic crops including rotation and cover crops such as rapeseed (Brassica napus), marigold (Tagetes spp.), forage pearl millet (Pennisetum typhoides), black-eyed Susan (Rudbeckia hirta), sudangrass (Sorghum bicolor) and sorghum-sudangrass were identified in the current project (LaMondia and Halbrendt, 2003). Native prairie plants that are resistant to M. hapla (LaMondia, 1996) may be useful as cover crops alone or in mixtures for managing this and other plant-parasitic nematode species. Furthermore, the incorporation of plant shoots as green manures appears to play a significant role in the nematode-antagonistic effects of many plants (Halbrendt, 1996; LaMondia and Halbrendt, 2003).


Biological control offers an alternative or supplemental management tactic to chemical or cultural management of plant-pathogenic nematodes. Pasteuria spp. are obligate, mycelial, endospore forming bacterial parasites of endoparasitic nematodes, such as RKN (Meloidogyne spp.), and several ectoparasitic nematodes, such as lesion (Pratylenchus) and sting nematodes (Belonolaimus) (Chen and Dickson, 1998; Giblin-Davis, 1990). These parasites are promising biological control agents for management of important agricultural species of Meloidogyne and Pratylenchus (Chen and Dickson, 1998). Pasteuria penetrans and Pasteuria thornei are widespread in soils in the southeastern USA where RKN and lesion nematode populations occur. However, we know comparatively little about their occurrence or ability to infect nematodes in more northern latitudes. However, we do know that Pasteuria occurs in northern climates because it has been reported on stunt nematodes from turf soil samples taken from Massachusetts (Wick and Dicklow, 2001), on lesion nematodes from potato fields in Minnesota (Oliveira et al., 2015), on soybean cyst nematode in Illinois (Atibalentja et al., 1998), and it also has been observed onfrom M. hapla in Connecticut and New York (LaMondia and Abawi, unpublished) and Michigan (Melakeberhan and Chen, unpublished).


Isolates of P. penetrans vary markedly in their specificity towards different RKN species and even to populations within species, however we know little regarding specificity. P. thornei and P. penetrans can reduce RKN populations below economic threshold levels in several different crops and environments (Chen and Dickson, 1998). More than 35 publications report that Pasteuria may reduce symptoms or disease severity caused by RKN in various crops (Chen and Dickson, 1998). In Florida, RKN and sting nematode suppression has been attributed to P. penetrans (Dickson et al., 1994; Chen et al., 1997; Weibelzahl-Fulton et al., 1996) and Candidatus pasteuria usga, respectively (Giblin-Davis, 1990).


As the density of soilborne endospores of a particular species and strain of Pasteuria increases, those soils may become more suppressive to nematodes susceptible to infection by that species and biotypes of Pasteuria. The molecular basis for host recognition and attachment is related to the formation of a glycoprotein adhesion formed late in the sporulation process in the nematode host (Brito et al., 2006). A monoclonal antibody to an epitope unique to this adhesion has provided a molecular probe to detect and quantify endospores in the soil and in planta (Schmidt et al., 2004). Both vegetative cells as well as spores of lines of Pasteuria penetrans showing preference for different Meloidogyne hosts may be detected by PCR using primers specific to genes for these lines (Schmidt et al., 2005). Molecular probes have been developed with monoclonal antibodies and specific gene probes to quantify endospores in the soil and in planta (Schmidt et al., 2004; Schmidt et al., 2005). Selective gene sequencing for different lines of Pasteuria penetrans have SNP’s used to distinguish lines on the basis of host preference (Nong et al., 2007). These approaches can now be applied to define the molecular basis of host preference and to explore the adaptation of lines of different Pasteuria spp. for maximal virulence toward a specific nematode host. Special emphasis is needed on Pasteuria thornei in that this bacterium is reported to be specific to Pratylenchus spp., which is a main target pathogen for this regional project. Very little information is available on this bacterium regarding its specificity, host range, or adaptability to northeastern climates.


Other microbial pest management agents such as Arthrobotrys, Bacillus, Burkholderia, Hirsutella, Paecilomyces, Paenobacillus, and Pochonia, may be used to enhance systems for the management of plant-parasitic nematodes (Kerry, 1998; Kokalis-Burelle et al., 2000; Meyer et al., 2001; Sikora and Hoffmann-Hergarten, 1993; Siddiqui and Mahmood, 1996; 1999; Stirling, 1991). In addition, natural products from nematode-antagonistic microbes can be toxic to plant-parasitic nematodes or disrupt the nematode life cycle (Anke and Sterner, 1997; Anke et al., 1995; Chen et al., 2000; Hallman and Sikora, 1996; Han and Ehlers, 1999; Hu et al., 1999; Köpcke et al., 2001; Meyer et al., 2000; Singh et al., 1991). Active compounds that affect egg hatch and second-stage juvenile mobility of M. incognita and Heterodera glycines were identified from nematode-associated fungi and from rhizosphere-inhabiting bacteria and fungi (Nitao et al., 1999; Meyer et al., 2000). Continued research is needed to identify additional microbes with ability to produce compounds active against plant-parasitic nematodes. These compounds have potential for application as novel nematicides, and the microbes that produce them as live biocontrol agents.


Cultural and biological approaches to nematode management may have numerous impacts on crop yield and sustainability beyond their impact on target plant-parasites. The success of cultural and biological control of plant-parasitic nematodes is usually evaluated based on the direct impact of management tactics on target nematode populations. However, the integration of crop rotations, cover crops, organic amendments, tillage practices, and other crop protection practices may have dramatic non-target effects on the physical, chemical and biological characteristics of soils. These non-target effects may substantially influence plant growth and yield. The concept of soil health uses certain characteristics such as low numbers of plant pests and pathogenic organisms, as well as high abundance of organisms that promote plant growth, such as the majority of non-pathogenic soil nematodes (Magdoff, 2001).


Current concerns of global climate change, pollution and soil loss are prompting a renewed look at ecology of soil nematodes in arable soils for alternative and effective strategies in disease management and plant nutrition. Nematodes contribute bioavailable nitrogen directly through excretion and indirectly through grazing, dispersal and immobilization of microbes (Freckman 1988). Bacterial feeding nematodes contribute 4 to 22% of net nitrogen bioavailability in forest soils (Neher et al. 2012). The contribution is inversely proportional to disturbance intensity.


In nematology, knowledge of plant-pathogenic nematodes of economic or quarantine importance is orders of magnitude greater than that of free-living or beneficial nematodes that comprise up to 60 to 80% of the community. Since 1988, the concept of nematodes as soil quality indicators and their predictive use in soil management represents a tremendous shift in emphasis in the discipline of nematology (Freckman 1988, Ferris 1993). Formerly, nematology was primarily a science focused on the management of parasitic and harmful plant pathogenic species. Currently, nematodes are also recognized as an integral and potentially useful component of soil systems.


Soil disturbance, be it physical or chemical, can have numerous effects on the composition of soil invertebrate communities. For example, soil compaction reduces soil porosity, destructive to soil communities both destroying habitat and eliminating natural predators (Moore and de Ruiter 1991). Chemical disturbance including amendments for fertility, organic matter, and pesticides lead to a general enrichment phenomenon (Neher 2001) and favor the bacterial channel (Yeates 1999). A combination of cultivation and fertilizer reduce the flow through the fungal channel (Bostrom & Sohlenius 1986).


Organic management often relies on intensive tillage to manage weeds, yet this practice may neutralize the biological benefits of organic amendments for fertility and pest management. Because soil organisms are difficult to see, farmers have little understanding of how management practices, such as tillage and cover crops, directly impact the composition and function of beneficial soil biota. The successional status of a soil community may reflect the history of disturbance. Less disturbance allows for soils to perform ecological functions of decomposition and nutrient cycling, which are desirable traits of healthy soil. Succession in cropped agricultural fields begins with depauperate soil after cultivation and clearing of unwanted vegetation that acts like an island to which organisms immigrate. First, opportunistic species, such as bacteria and their predators, are colonists of soil. Communities become dominated by organisms with short generation times, small body size, rapid dispersal and generalist feeding habits such as by bacteria and bacterivorous nematodes. Subsequently, fungi and fungivorous nematodes migrate into the area. Secondary and tertiary consumers or predators establish later. Indices of ecological succession are more reliable in detecting statistical differences than relative abundance or individual trophic groups (Neher et al. 1995).


Different species exhibit contrasting levels of sensitivity or tolerance to disturbance because of unique survival and/or reproductive traits. For example, conventional tillage can reduce ratios of amoebae to flagellate protozoa and oribatid- to astigmatid mites (Zhang et al., 2012; Socarrás 2013). Two variations of these indices have been employed successfully for nematodes: Maturity index is a weighted mean of abundance of taxa at different states of ecological succession (Bongers 1990); channel and structural indices are subsets of the maturity index that reflect early and late succession, respectively (Ferris et al. 2001). Ratio of fungivorous to bacterivorous nematodes similarly reflects the succession phase of decomposition. In both cases, smaller values reflect more recent or greater intensity disturbance. These measures are indicators of soil degradation (Paoletti et al. 2007).


Additions of organic matter, such as compost, are considered beneficial for vegetable cropping systems because they contribute positively to promote plant growth, increase yield, and suppress disease. Compost research is among the top five research priorities identified by the Organic Farming Research Foundation (Sooby et al. 2007). Composted organic wastes can serve as a biological inoculant for field soils to reduce the severity of root diseases. We know the microbiology differs among compost recipes and production processes (Neher et al. 2013) but neither the ecological function nor mechanisms have been described for these microbial communities (Mazzola 2004). With a better understanding of the microbiology of organic amendments, we can learn the pivotal points where it can be managed to enhance disease suppressiveness either by regulating the microbe-microbe interactions or microbe-plant interactions in soil.


The link between healthy soils and healthy plants remains fundamental to ecologically based pest management. Adequate moisture, good soil tilth, appropriate pH, appropriate amounts and balance of nutrients and diverse and active communities of soil organisms all promote vigorous plants that are tolerant to insect damage and disease (Magdoff & van Es 2010).


Biological indicators are underrepresented in programs designed to measure health of agricultural soil, e.g., Cornell Soil Health Assessment (Gugino et al. 2009) which has major impact and adoption in the northeastern US. While it provides useful information on the chemical and physical components of soil, it places little emphasis on soil biology; focusing solely on root health in terms of overall vigor and damage by root pathogens such as Fusarium, Pythium, or Rhizoctonia. Microbes and organic matter are the most commonly employed, but are difficult to interpret because of their spatial and temporal variation. Therefore, it makes more sense to move up the food chain to secondary, tertiary or quaternary consumers. They integrate all levels of food chain below and chemical/physical factors, and sometimes present top or keystone predators (Neher 2001). Although chemistry and microbial biomass are correlated with nematode community indicators, they explain only 23% of variation of soil nematode community composition (Neher and Campbell 1994). Nematode community indices are useful tools to both assess the impact of agricultural management practices on nematode community structure dynamics and add to soil health toolkits calibrated by geographic region and specific agronomic and horticultural production systems. Interpretation requires a baseline database of these indices calibrated by ecoregion (Neher et al. 1997) and ecosystem type (Neher et al. 2005). Initial efforts demonstrated the utility of successional based indices to quantify effects of cultivation (Freckman and Ettema 1993, Neher et al. 1995), application of organic amendments (Neher 1999), contamination by polycyclic aromatic hydrocarbons (Blakely et al. 2002) and heavy metals (Korthals et al. 1996, 1998), maturation of compost (Steel et al. 2009), and establishment of biological soil crust (Darby et al. 2007). A long-term goal is to add a biological indicator representing beneficial soil invertebrates to the Cornell Soil Health Assessment. This adds a component that measures ecological function and environmental impact, which are interdependent with productivity to achieve sustainable intensive production systems.

Objectives

  1. Develop and integrate management tactics for control of plant-parasitic nematodes including biological, cultural (such as rotation or cover crops and plant resistance), and chemical controls.
  2. Determine the ecological interactions between nematode populations, nematode communities, ecosystems and soil health.
  3. Outreach and communication - Compile and present/ publish guidance on nematode management and management effects on soil health for different crops under different conditions.

Methods

Objective 1. Develop and integrate management tactics for control of plant-parasitic nematodes including biological, cultural (such as rotation or cover crops and plant resistance), and chemical controls.

Biological The identification of nematode-suppressive soils or new combinations of nematode species such as Meloidogyne hapla, Pratylenchus penetrans and several turf nematodes with biocontrol agents is the first necessary step in the development of new nematode management tactics. Soil samples will be collected from fields in various geographic regions and cropping systems, especially fields with known decline of nematode population densities. The soils will be bioassayed in the greenhouse for their levels of suppressiveness to major plant-pathogenic nematode species such as M. hapla, Pr. penetrans, and H. glycines present in the fields, following the procedures developed in previous studies (Chen, 2007; Pyrowolakis et al., 2002; Robinson et al., 2008; Weibelzahl-Fulton et al., 1996; Westphal, 2005; Westphal et al., 2011). Strains (biotypes) of Pasteuria penetrans have been isolated with preference for different races of M. arenaria, M. incognita, and M. javanica (Ostendorp et al., 1991; Chen and Dickson, 1998). Members of this project (CT, RI, MA, WV, MI, MN) will collaborate to identify and document populations of plant parasitic nematodes associated with Pasteuria and evaluate the impact of this biocontrol organism on disease. Collaboration with Drs. Dickson and Burelle in FL may identify new strains or species of Pasteuria not currently produced as nematode biological control agents by industry. Members of this project already have collected a number of Pasteuria isolates that can be tested on nematode species Pratylenchus spp. and M. hapla. For example, Pasteuria collected from Pratylenchus and free-living nematodes in MN will be tested for specificity to plant-parasitic nematode species and populations. The Pasteuria populations will be tested in vitro for their attachment of endospores to the nematodes of different populations of Pratylenchus and H. glycines J2 (de Gives et al., 1999). Numerous fungi have been isolated from nematodes in suppressive sites will also be tested for biological control potential (Chen and Liu, 2005; Liu and Chen, 2005). Research results from the current project suggest that there may be specificity in Pasteuria attachment and infection between Meloidogyne hapla populations from different regions, namely Connecticut and Florida.

Cultural Nematode management with plant resistance, crop rotation, winter cover crops or biofumigation crops has been difficult to achieve, but progress has been made and additional research is under way. Plant resistance to nematodes of economic concern in the northeast has not been available. Recently, pepper (Capsicum spp.) lines developed from the U.S. Capsicum collection (USDA, ARS) have been identified with moderate resistance to M. hapla. There may also be potential for resistance in accessions of cowpea. Evaluation of these plants against different populations of M. hapla and other genera of importance, particularly lesion and dagger nematodes, remains to be investigated. In addition, winter annual oilseed pennycress germplasm lines collected throughout the USA will be screened for their susceptibility and resistance to various H. glycines populations in MN. Greenhouse and field studies will be conducted to determine location-specific interactions of Meloidogyne hapla and emerging resistant carrot cultivars in diverse soil types and the presence of suppressive soils in Michigan.

Members of NE-1040 identified nematode-antagonistic rotation and cover crops including rapeseed (Brassica napus), marigold (Tagetes cpp), forage and grain pearl millet (Pennisetum typhoides), Rudbeckia hirta, sudangrass (Sorghum bicolor) and sorgho-sudangrass. No single plant was effective against all plant-parasitic nematodes in the Northeast. Some plants were more practical than others as rotation or cover crops due to agronomic traits, ability to compete with weeds (which are often hosts of the target nematodes) and ability to fit into cropping systems. Our proposed research will evaluate whether mixtures or series of rotation crops with different modes of action may be more effective against multiple genera of plant parasitic nematodes which often occur in the same field. Aster and Rudbeckia are resistant to M. hapla (LaMondia, 1997), and Rudbeckia and marigold reduced lesion nematode densities and potato early dying. However, these crops are difficult to establish as a monoculture. In addition, Rudbeckia was a good host for dagger nematodes. Combining Aster and Rudbeckia with grasses such as sudangrass or millet may increase efficacy against a wider range of nematodes. The incorporation of plant shoots as green manures in rotation periods prior to replanting orchards also may impact the nematode-antagonistic effects of these plants (Halbrendt, 1996; LaMondia and Halbrendt, 2003). Dagger nematodes (Xiphinema spp.) remain one of the most important nematode pests in tree fruit production because of their ability to transmit virus pathogens from plant to plant. The absence of effective chemical nematicides is a significant constraint to production in infested orchards, especially for peach, cherry and nectarine. While new biocontrol agents for plant-parasitic nematodes have been registered in recent years, efficacy against dagger nematode is limited (Kotcon, unpublished), demonstrating that management practices for one pest-crop combination cannot always be transferred to others. Use of tall fescue and brassica rotation crops have demonstrated some efficacy in suppressing dagger nematode at orchard establishment (Biggs, et al., 1997; Panaccione, et al., 2006; Kotcon and Batchelor, 1992), but these have not been demonstrated in bearing tree fruit orchards. Trials to evaluate nematode suppressive cover crops (brassicas, sunn hemp, and tall fescue) will be established in dagger nematode-infested peach orchards in WV.

A significant number of combinations need to be investigated as summer rotation or winter cover crops. Winter cover crops may serve as nematode-trapping crops or their residue may affect nematodes in the following season. Studies will be conducted in multiple states to determine the effects of cover crops and rotation systems on nematode populations. Horticultural and field cropping systems and tillage practices in field cropping systems will be evaluated for impacts on nematode community, soil health and crop yield in different soil types in either experiment station and/or collaborating grower fields of Michigan. Finally, the effects of biofumigation or cropping systems on plant parasitic nematodes is important under this objective, but impacts on soil nematode communities will also be investigated under Objective 2.

Chemical A number of new nematicidal compounds are under development and research will be required to first evaluate efficacy and then to integrate these materials into effective management systems. This will be done on turf in MA and RI and for other crops in CT. Research on botanical nematicides will be conducted in TN. Many nematicidal non-microbial products are based on neem or sesame oils (50%) or saponins from Quillaja saponaria (40%). Since chenopods have both oils and saponins with the potential to retard nematode growth and reproduction, development of products from these sources would increase strategies for nematode control in sustainable and organic systems.

Oil of epazote (Dysphania ambroisioides; Mexican wormseed), a culinary chenopod herb, is used for management of arthropods and deworming animals and humans. Epazote and other chenopods produce potent nematicidal saponins and ascaridole (a terpene), and development of the root-knot nematode Meloidogyne incognita (Mi) is severely impaired in epazote roots. We hypothesize that chenopods contain unique saponins and other secondary metabolites suitable for biopesticide development, and that delivery systems can be developed to provide safe and effective nematode management. The main goal is to develop a botanical nematicide from the goosefoot or chenopod plant family (Chenopodiaceae).

Anti-nematode activity. Toxicity of extracts to nematodes will be screened in vitro against Meloidogyne incognita (Mi), Rotylenchulus reniformis (Rr), and Aphelenchoides fragariae (Af) with tests designed for Mi (Rehman et al. 2013) and Pratylenchus scribneri (Kimmons et al. 1989). Aphelenchoides fragariae is a plant-parasitic nematode that can be maintained in culture with fungi (Jagdale and Grewal 2006). Meloidogyne incognita (tomato) and R. reniformis (cantaloupe) are currently maintained in the greenhouse. Bacteria-feeding rhabditids may be used for preliminary testing and screening (McDonald et al. 2004) due to their high rate of reproduction.

Direct effect of epazote and related species. Colonization of epazote and other Chenopodiaceae by root-endoparasitic nematodes (Mi and Rr) will also be determined; in preliminary tests, life cycles of Mi were abbreviated or disrupted in epazote due to local malformation and disruption of vessels in the forming gall (Bernard & Long 2009). Nematode development and reproduction was severely reduced when epazote was the host plant. Companion plantings of epazote and M. incognita-susceptible plants will be made to determine if presence of epazote roots affects invasion of adjacent susceptible roots.

Extracts and chenopod mulches as nematicidal treatments. Bioactive extracts identified from in-vitro tests will be tested as soil drenches for Mi management. Chenopods identified as poor hosts for Mi will be produced in sufficient mass to incorporate into Mi-infested soil planted with tomato, and roots will be analyzed for nematode invasion and galling (both in greenhouse and field experiments). Bioactive extracts will be applied to hosta and chrysanthemum as foliar sprays to manage Af. Phytotoxicity and efficacy against Af infection will be determined.

 

Objective 2. Determine the ecological interactions between nematode populations, nematode communities, ecosystems and soil health.

Two focal areas will be addressed in this project:

  1. Effect of cover, trap or rotation crops influence soil biology (Connecticut, Michigan, West Virginia)

Soil health change among alternative management systems will be measured at key long-term research sites such as the Michigan State University, Long-Term Ecological Research site at the Kellogg Biological Station and at the West Virginia University Organic Research Farm. Treatments in Michigan will include cover crops, trap crops and rotation crops (Melakeberhan et al. 2015, Melakeberhan and Avendaño 2008). These data will add to previous nematode community testing at these sites (Freckman and Ettema 1993). In West Virginia, treatments will include crop rotations and compost amendments (Kotcon and Batchelor 1992). Monitoring will continue on transitions away from fumigation and chemical management to crop rotation on strawberry in Connecticut (LaMondia et al. 2005). At all locations, soil health assessment will include nematode community succession and parameters that characterize chemical and/or physical properties of soil including water stable soil aggregates (Cambardella and Elliott 1994), soil carbon-nitrogen (Nyiraneza 2003), and particulate organic matter (Cambardella and Elliott 1992). Taxonomic genera will be assigned to a trophic group according to Yeates et al. (1993). Indices of successional maturity and food web complexity (by trophic diversity) will be computed (Neher and Darby 2006).

Turfgrasses are highly susceptible to damage by plant-parasitic nematodes.  Consequently, a significant amount of research has been undertaken in multiple regions of the United States to determine factors such as damage thresholds, important parasitic species, physical and chemical factors influencing nematode population growth and seasonal variation in plant-parasitic population numbers (Jordan and Mitkowski, 2006; McClure et al., 2012; Settle et. al., 2007; Sikora et al., 2001; Walker et al., 2002).  However, little work has been undertaken to examine factors that influence other ecological nematode communities in putting greens and other turfgrass systems. It has been documented that organically managed turfgrasses typically sustain fewer plant-parasites and higher levels of bacterivores but it is unclear exactly which management factors contribute to the observed differences (Allan et al., 2014; Zhao et al., 2011).  It is extremely difficult to manage golf course turf organically and a widespread switch to organic management practices seems unlikely.  However, the determination of which factors directly correlate to the differences between the two systems would allow the incorporation or avoidance of management practices that reduce microbial diversity, specifically as it relates to nematode populations.  By understanding how specific practices impact different nematode communities, those practices could be altered without changing an entire management system.  The two most obvious differences between organic and conventional golf course management is the type of fertilizer used (organic vs. synthetic) and the application of fungicides on a biweekly basis, which are not employed in organic systems.  Rhode Island researchers will examine the effects of varied rates and types of fungicides, in addition to the effect of organic vs synthetic fertilizers, on the population dynamics of plant-parasitic nematodes and bacterivores on golf course putting greens.

  1. Basic ecology and mechanisms of beneficial organisms: microbe-microbe, plant-microbe, plant-microbe-invertebrate interactions (New York, Minnesota, Vermont)

The effects of long-term corn-soybean crop sequences on plant-parasitic nematode community, microbial community, soil health, and corn and soybean yield will be studied in a field site that was established in 1982 in Minnesota (Crookston et al. 1991). This is a unique long-term crop rotation research site in the corn-soybean production systems in the region. The crop sequences are: (i) five-year rotation of each crop such that both crops are in years 1, 2, 3, 4, and 5 of monoculture every year; (ii) annual rotation of each crop with both crops planted each year; (iii) continuous monoculture of each crop; (vi) annual rotation of two different cultivars of each crop. The role of plant-pathogenic nematodes of crop rotation effect on crop yields and the crop sequence effect on soil nematode community have been investigated (Grabau and Chen, 2016a, b, c) The diversity and function of the microbial community under various long-term cropping systems will be determined by quantification of different groups of microbes, and analysis of phylogenetic relationships among them. The relationship between the microbial community, plant-parasitic nematodes, soil health, and crop productivity measured as crop yields will be analyzed. Vermont will continue to evaluate the fungal and bacterial aspects of suppressive soils with the aim of narrowing in on mechanisms of natural suppression of SCN in collaboration with Minnesota. Composts of known recipe and process will be evaluated for mechanisms associated with suppression of disease (Neher et al. 2015). Composts provide a nutritious substrate and habitat to support beneficial microbes and predaceous invertebrates analogous to a probiotic for soil. Moving up one level in the food chain, investigations in New York will focus on the effects of soil meso- and macrofauna on nematodes via predation and impacts on soil properties (Wickings and Grandy 2013). These data are necessary for calibrate and interpret an indicator of beneficial soil invertebrates in the Cornell Soil Health Assessment.

 

Objective 3. Outreach and communication - Compile and present/ publish guidance on nematode management and management effects on soil health for different crops under different conditions.

The methodology for Objective 3 consists of four components, each designed to serve the needs the crop/plant producers, agribusiness professionals, government agency personnel and Extension educators of the Northeast Region: 1) Nematology Short Courses held in conjunction with the Annual Meeting of the Regional Research Technical Committee, 2) Nematology Webinar Series to provides crop consults and other plant professionals with nematology education opportunities and formal professional credits, 3) Project participants will work together to obtain outside funding to enable the development of a GoTo Nematology Website to provide specific information on The Role of Plant-parasitic Nematodes and Nematode Management in Biologically Based Agriculture and 4) Other associated outreach activities of the members of the Technical Committee.

  • Annual Short Course (Each short course will have sections and nematodes, soil health, cover crops and bio-based farm management).
    • Turf grass nematodes and management (Rhode Island, October 2017)
      • Mitkowski
    • Agronomic crop nematodes and management (Delaware, October 2018)
      • Sherrier
    • Ornamental and nursery crop nematology (Connecticut, October 2019)
      • LaMondia
    • Vegetable crop nematodes and management (Massachusetts, October 2020)
      • Wick
    • Tree fruit and small fruit nematology (West Virginia, October 2021)
      • Kotcon
  • Featured Nematode Webinar Series
    • Nematodes: A Practical Overview (2017)
      • Bird and Dickson
    • Soil Health and Bio-Based Systems (2018)
      • Neher and Grigar (USDA/NRCS/MI)
    • Cover Crop Impacts and Management (2019)
      • LaMondia and Abawi
    • Resistant and Tolerant Cultivars for Nematode Management (2020)
      • Thies
    • Biological Control of Plant Parasitic Nematodes (2021)
      • Phelan
  • Regional Nematode Website. Project participants will work together to obtain outside funding to enable the development of a website to increase outreach efforts.
    • This high quality GoTo Website will be developed in 2017, including alpha and beta testing associated with the 2017 Short Course and Webinar, respectively.
    • Information from the Short Courses, Webinar Series, project research results and other information from the members or the Technical will serve as the basis for the Website.
    • The Website will be constructed in a way that it can be modified on a real-time basis. In addition, it will be reviewed quarterly.

Measurement of Progress and Results

Outputs

  • Baseline calibration data for effect of cover, trap and rotation crops Comments: The Cornell Soil Health Assessment (Gugino et al. 2009) has major impact and adoption in the northeastern US. While it provides useful information on the chemical and physical components of soil, it places little emphasis on soil biology; focusing solely on root health in terms of overall vigor and damage by root pathogens such as Fusarium, Pythium, or Rhizoctonia.
  • Produce a reference booklet that provides an overview of beneficial soil organisms, their ecological functions, and soil management practices that promote their abundance and activity (New York, Vermont)

Outcomes or Projected Impacts

  • Better soil health management practices
  • Rotation systems that reduce plant damage from pathogenic nematodes and increase soil health parameters
  • A long-term goal is to add a biological indicator representing beneficial soil invertebrates to the Cornell Soil Health Assessment.

Milestones

(2017):<ul><li>Meloidogyne hapla-resistant pepper will be supplied to cooperators and tested against nematode populations. <li>Test location-specific traits relative to M. hapla populations in greenhouse <li>Evaluate the effects of identified non-host or antagonistic rotation crops against different nematodes in multiple states under field conditions. <li>Identify nematode suppressive soils <li>Identify and define host-specific association of Pasteuria spp. toward plant parasitic nematode hosts in suppressive soils. <li>Evaluate new nematicidal products for efficacy <li>Approach soil scientists from collaborating institutions and engage them in participating in lines of research focusing on microbial communities in soil. <li>Conduct grower education, annual short course and webinar <li>Investigate the relationship between the microbial community, plant-parasitic nematodes, soil health, and crop productivity</ul>

(2018):<ul><li>Verify location-specific traits relative to M. hapla populations in the field <li>Test suppressive soils for potential nematode management practices <li>Adjust cover- and rotation-crop experimental designs based on previous results <li>Continue cover- and rotation-crop experiments <li>Evaluate new nematicidal products for efficacy <li>Investigate the relationship between the microbial community, plant-parasitic nematodes, soil health, and crop productivity <li>Conduct grower education, annual short course and webinar</ul>

(2019):<ul><li>Repeat location-specific traits relative to M. hapla populations in the field <li>Continue testing suppressive soils for potential nematode management practices <li>Continue cover- and rotation-crop experiments <li>Determine the relationship between the microbial community, plant-parasitic nematodes, soil health, and crop productivity <li>Integrate effective new nematicidal products into management systems <li>Publish preliminary results <li>Conduct grower education, annual short course and webinar</ul>

(2020):<ul><li>Develop lines of Pasteuria spp. with enhanced virulence toward specific RKN and lesion nematodes. <li>Analyze and publish location-specific traits relative to M. hapla populations <li>Analyze and publish suppressive soils for potential nematode management practices <li>Conclude and evaluate long-term impacts of cover - and rotation-crop experiments <li>Determine the relationship between the microbial community, plant-parasitic nematodes, soil health, and crop productivity <li>Integrate effective new nematicidal products into management systems <li>Publish preliminary results <li>Conduct grower education, annual short course and webinar</ul>

(2021):<ul><li>Analyze data, present reports at stakeholder and professional meetings, and publish results in peer-reviewed journals. <li>Publish a web-based fact sheet comparing the efficacy of different rotation and cover crops against lesion, root-knot and dagger nematodes. <li>Conduct grower education, annual short course and webinar</ul>

Projected Participation

View Appendix E: Participation

Outreach Plan

Associated outreach activities of the members of the Technical Committee.



  • Annual Short Course (Each short course will have sections and nematodes, soil health, cover crops and bio-based farm management).

    • Turf grass nematodes and management (Rhode Island, October 2017) - Mitkowski

    • Agronomic crop nematodes and management (Delaware, October 2018) - Sherrier

    • Ornamental and nursery crop nematology (Connecticut, October 2019) - LaMondia

    • Vegetable crop nematodes and management (Massachusetts, October 2020) - Wick

    • Tree fruit and small fruit nematology (West Virginia, October 2021) - Kotcon




  



  • Featured Nematode Webinar Series


    • Nematodes: A Practical Overview (2017) - Bird and Dickson

    • Soil Health and Bio-Based Systems (2018) - Neher and Grigar (USDA/NRCS/MI)

    • Cover Crop Impacts and Management (2019) - LaMondia and Abawi

    • Resistant and Tolerant Cultivars for Nematode Management (2020) -Thies

    • Biological Control of Plant Parasitic Nematodes (2021) - Phelan




  • Regional Nematode Website. Project participants will work together to obtain outside funding to enable the development of a website to increase outreach efforts.

    • This high quality GoTo Website will be developed in 2017, including alpha and beta testing associated with the 2017 Short Course and Webinar, respectively.




 


Information from the Short Courses, Webinar Series, project research results and other information from the members or the Technical will serve as the basis for the Website.

Organization/Governance

The technical committee will consist of at least one voting member from each of the participating states (Attachment A), the administrative advisor, and the NIFA representative. The technical committee will elect a chairperson, secretary, and at least one member-at-large to serve as an executive committee that will serve two years. The regional Technical committee will meet annually to report on the research results obtained, discuss and exchange information and ideas and to plan and coordinate next year’s work relating to the objectives of this proposal. A coordinator for each of the objectives may be designated to facilitate the coordination and reporting of the research being conducted by the collaborators. The technical committee may invite other scientists with experience in biological control, crop production systems, integrated pest management, sustainable agricultural practices, and others to participate in the annual meeting to provide specific information and strengthen the discussion.

Literature Cited

Allan E, Manter D, Jung G 2014. Comparison of nematode communities between organically and conventionally managed golf courses. Phytopathology 105:S1.5


Allen VG, MT Baker, E Segarra, CP Brown 2007. Integrated irrigated crop‐livestock systems in dry climates. Agron J 99:346‐360.


Allen VG, CP Brown, E Segarra, CJ Green, TA Wheeler, V Acosta‐Martinez, TM Zobeck 2008. In search of sustainable agricultural systems for the Llano Estacado of the U.S. Southern High Plains. Agric Ecosyst Environ 124:3‐12. Alumai A, Parwinder GS, Hoy CW, Willoughby DA (2006). Factors affecting the natural occurrence of entomopathogenic nematodes in turfgrass. Biocontrol 36:3, 368-374.


Alumai A, Parwinder GS, Hoy CW, Willoughby DA 2006. Factors affecting the natural occurrence of entomopathogenic nematodes in turfgrass. Biocontrol 36:3, 368-374.


Anke, H., M. Stadler, A. Mayer, and O. Sterner. 1995. Secondary metabolites with nematicidal and antimicrobial activity from nematophagous fungi and Ascomycetes. Canadian Journal of Botany 73: S932-S939.


Anke, H., and O. Sterner. 1997. Nematicidal metabolites from higher fungi. Current Organic Chemistry 1: 361-374.


Atibalentja, N., Noel, G. R., Liao, T. F., and Gertner, G. Z. 1998. Population changes in Heterodera glycines and its bacterial parasite Pasteuria sp. in naturally infested soil. Journal of Nematology 30:81-92.


Avendaño, F., Schabenberger, O., Pierce, F.J. & Melakeberhan, H. 2003. Geostatistical analysis of field spatial distribution patterns of soybean cyst nematode. Agronomy Journal 95, 936-948.


Beare MH, Brussaard L, Ferrera-Cerrato R 1997. Fungal and bacterial pathways of organic matter decomposition and nitrogen mineralization in arable soil. Pp. 37-70 in: Brussaard L, Ferrera-Cerrato R (eds) Soil Ecology in Sustainable Agricultural Systems, Lewis, Boca Raton, LA.


Biggs, A. R., T. A. Baugher, J. B. Kotcon, D. M. Glenn, A. R. Collins, A. J. Sexstone, H. W. Hogmire, and R. E. Byers. 1997. Growth of apple trees, populations of nematodes, voles, and orchard floor weeds, and nitrate mobility following a corn versus fescue crop rotation. American Journal of Alternative Agriculture 12:162-172.


Bongers, T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologica 83, 14-19.


Bongers, T. & Ferris, H. 1999. Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology and Evolution 14, 224-228.


Bongers, T., Van der Meulen, H. & Korthals, G. 1997. Inverse relationship between the nematode community maturity index and plant parasite index under enriched nutrient conditions. Applied Soil Ecology 6, 195-199.


Brito, J. A, J. F. Preston, D. W.Dickson, R. M. Giblin-Davis, D. S. Williams, H. C. Aldrich, and J. D. Rice. 2003. Temporal Production and Immunolocalization of an Epitope During Pasteuria penetrans sporogenesis. Journal of Nematology 35(3):278-288.


Blakely JK, Neher DA, Spongberg AL 2002. Microinvertebrate and microbial communities, and decomposition as indicators of polycyclic aromatic hydrocarbon contamination. Appl Soil Ecol 21:71-88.


Bommarco,R.,Kleijn,D.,and Potts,S.G. 2013. Ecological intensification: harnessing ecosystem services for food security. Trends Ecol. Evol. 28,230–238. doi:10.1016/j.tree.2012.10.012


Bongers T 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14-19.


B`strom S, Sohlenius B. 1986. Short-term dynamics of nematode communities in arable soil: Influence of a perennial and an annual cropping system. Pedobiologia 29:345-357.


Cambardella CA, Elliott ET 1994. Carbon and nitrogen dynamics of soil organic matter fractions from cultivated grassland soils. Soil Sci Soc Am J 58:123130.


Cambardella CA, Elliott ET 1992. Particulate soil organic-matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777782.


Chaparro JM, Sheflin AM, Manter DK, Vivanco JM 2012 Manipulating the soil microbiome to increase soil health and plant fertility. Biol. Fertil. Soils 48: 489-499.


Chappell,M.J., and Lavalle,L.A. 2011.Food security and biodiversity: can we have both? An agroecological analysis. Agric. Hum. Values 28,3–26.doi: 10.1007/s10460-009-9251-4


Chen, S. Y. 2007. Suppression of Heterodera glycines in soils from fields with long-term soybean monoculture.  Biocontrol Science and Technology 17:125-134.


Chen, S. Y., D. W. Dickson, and D. J. Mitchell. 2000. Viability of Heterodera glycines exposed to fungal filtrates. Journal of Nematology 32: 190-197.


Chen, Z. X. and D. W. Dickson. 1998. Review of Pasteuria penetrans: Biology, ecology, and biological control potential. Journal of Nematology 30:313-340.


Chen, Z. X., D. W. Dickson, D. J. Mitchell, R. McSorley, and T. E. Hewlett. 1997. Suppression mechanisms of Meloidogyne arenaria race 1 by Pasteuria penetrans. Journal of Nematology 29:1-8.


Crookston RK, Kurle JE, Copeland PJ, Ford JH, Lueschen WE 1991. Rotational cropping sequence affects yield of corn and soybean. Agron Jl 83:108-113.


Darby BJ, Neher DA, Belnap J 2007. Soil nematode communities are ecologically more mature beneath late- than early-successional stage biological soil crusts. Appl Soil Ecol 35: 203-212.


de Gives, P. M., Davies, K. G., Morgan, M., and Behnke, J. M. 1999. Attachment tests of Pasteuria penetrans to the cuticle of plant and animal pathogenic nematodes, free living nematodes and srf mutants of Caenorhabditis elegans. Journal of Helminthology 73:67-71.


Dickson, D. W., M. Oostendorp, R. M. Giblin-Davis, and D. J. Mitchell. 1994. Control of plant-parasitic nematodes by biological antagonists. Pp 575-601 in Pest Management in the tropics, Biological control-a Florida perspective. D. Rosen, F. D. Bennett and J. L. Capinera, eds. Intercept Ltd, U.K.


Doran, J.W. & Zeiss, M.R. 2000. Soil health and sustainability: managing the biotic component of soil quality. Applied Soil Ecology 15, 3-11.


Ferris, H. 2010. Contribution of nematodes to the structure and function of the soil food web. Journal of Nematology 42, 63–67.


Ferris, H., Bongers, T. & De Goede, R.G.M. 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 18, 13-29.


Ferris H 1993. New frontiers in nematode ecology. J Nematol 25:374-82.


Ferris H, Bongers T, de Goede RGM 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13-29.


Fiscus DA, Neher DA 2002. Distinguishing nematode genera based on relative sensitivity to physical and chemical disturbances. Ecol Appl 12:565-575.


Freckman DW 1988. Bacterivorous nematodes and organic-matter decomposition. Agric Ecosyst Environ 24:195-217.


Freckman DW, Ettema CH 1993. Assessing nematode communities in agroecosystems of varying human intervention. Agric Ecosyst Environ 45:239-261.


Giblin-Davis, R. M. 1990. Potential for biological control of phytoparasitic nematodes in berrmudagrass turf with isolates of the Pasteuria penetrans group. Proc. Fla. State Hort. Soc. 103:349-351.


Grabau, Z. J., and Chen, S. 2016a. Influence of long-term corn-soybean crop sequences on soil ecology as indicated by the nematode community.  Applied Soil Ecology 100:172-185.


Grabau, Z. J., and Chen, S. Y. 2016b. Determining the role of plant-parasitic nematodes in the corn-soybean crop rotation yield effect using nematicide application: I. corn.  Agronomy Journal 108:782-793.


Grabau, Z. J., and Chen, S. Y. 2016c. Determining the role of plant- nematodes in the corn-soybean crop rotation yield effect using nematicide application: I. soybean.  Agronomy Journal 108:1168-1179.


Gugino BK, Idowu OJ, Schindelbeck RR 2009. Cornell Soil Health Assessment Training Manual. 2nd ed. Cornell University. http://soilhealth.cals.cornell.edu/extension/manual.htm


Habteweld, A.W., Brainard, D., Ngouajio, M., Kravchenko, S., Grewal, P.S. & Melakeberhan, H. 2015. Integrating the concepts of fertilizer use efficiency (FUE) and nematode -based soil food web models for broader use in soil health management. 54th Annual Meeting of the Society of Nematologists Program Abstracts. 52.


Halbrendt, J. M. 1996. Allelopathy in the management of plant-parasitic nematodes. Journal of Nematology 28:8-14.


Hallmann, J., and R. A. Sikora. 1996. Toxicity of fungal endophyte secondary metabolites to plant-parasitic nematodes and soil-borne plant-pathogenic fungi. European Journal of Plant Pathology 102: 155-162.


Han, R. C., and R. U. Ehlers. 1999. Trans-specific nematicidal activity of Photorhabdus luminescens. Nematology, 1: 687-693.


Hu, K.J., J. X. Li, and J. M. Webster. 1999. Nematicidal metabolites produced by Photorhabdus luminescens (Enterobacteriaceae), bacterial symbiont of entomopathogenic nematodes. Nematology 1: 457-469.


Jordan KS, Mitkowski NA 2006. Population dynamics of plant-parasitic nematodes in golf course greens turf in southern New England. Plant Dis 90:4, 501-505.


Kerry, B. R. 1998. Progress towards biological control strategies for plant-parasitic nematodes. The 1998 Brighton Crop Protection Conference: Pests and Diseases 3:739-746.


Kokalis-Burelle, N., P. Fuentes-Bórquez, and P. Adams. 2000. Effects of reduced risk alternatives on nematode populations and crop yield. Proceedings of the Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions: 61.1-61.2.


Köpcke, B., D. Wolf, A. Heidrun, and O. Sterner. 2001. New natural products with nematicidal activity from fungi. British Mycological Society International Symposium, "Bioactive Fungal Metabolites – Impact and Exploitation" Abstract Booklet: p. 72.


Kotcon JB, Batchelor TP 1992. Population dynamics of Xiphinema spp. on rotation crops. J Nematol 24:603.


King, T. N. 2015. Investigations of Pasteuria and the Root-Lesion Nematode Pratylenchus penetrans in Soils Collected from Certified Organic Farms in the Mid-Atlantic United States. MS. Thesis. West Virginia University. Morgantown, WV.


LaMondia, J. A. 1996. Response of additional herbaceous perennial ornamentals to Meloidogyne hapla. Supplement to the Journal of Nematology 28 (4S):636-638.


LaMondia, J. A. and J. M. Halbrendt. 2003. Differential host status of rotation crops to dagger, lesion and rot-knot nematodes. Journal of Nematology 35.


LaMondia JA, Cowles RS, Los L 2005. Prevalence and potential impact of soil-dwelling pests in strawberry fields.  HortScience 40:1366-1370


Magdoff, F., and H. van Es. 2000. Building soils for better crops. 2nd edition, Sustainable Agric. Publ., University of Vt., Burlington, VT. 230 pp.


Maung, Z.T.Z., Poindexter, S., Clark, G., Stewart, J., Hubbell, L., & Melakeberhan, H. 2015. Effects of rotation and cover crops on nematode communities and soil health in different sugar beet production soils. 54th Annual Meeting of the Society of Nematologists Program Abstracts. 64.


Mazzola M 2004 Soil microbial community structure for disease suppression. Annu Rev Phytopathol 42:35-59.


McClure MA, Nischwitz C, Skantar AM, Schmitt ME, Subboti SA 2012. Root-knot nematodes in golf course greens of the Western United States. Plant Dis 96:5, 635-647.


McSorley, R. 1998. Alternative practices for managing plant-parasitic nematodes. Amer. J. Alternative Agriculture 13:98-104.


McSorley, R. 1999. Host suitability of potential cover crops for root-knot nematodes. Supplement to the Journal of Nematology 31:619-623.


McSorley, R. and D.W. Dickson. 1995. Effect of tropical rotation crops on Meloidogyne incognita and other plant-parasitic nematodes. Supplement to the Journal of Nematology 27:535-544.


McSorley, R. and R.N. Gallaher. 1992. Comparison of nematode population densities on six summer crops at seven sites in north Florida. Supplement to the Journal of Nematology 24:699-706.


McSorley, R., Dickson, D. W., de Brito, J. A., Hewlett, T. E., and Frederick, J. J. 1994. Effects of tropical rotation crops on Meloidogyne arenaria population densities and vegetable yields in microplots. Journal of Nematology 26:175-181.


Melakeberhan H, Wang W, Kravchenko A, Thelen K 2015. Effects of agronomic practices on the timeline of Heterodera glycines establishment in a new location. Nematology 17:705-713. DOI: 10.1163/15685411-00002903.


Melakeberhan, H., Wang, W., Kravchenko, A. & Thelen, K. 2015. Effects of agronomic practices on the timeline of Heterodera glycines establishment in a new location. Nematology 17, 705-713. DOI: 10.1163/15685411-00002903.


Melakeberhan, H., & Avendaño, M.F. 2008. Spatio-temporal consideration of soil conditions and site-specific management of nematodes. Precision Agriculture, 9: 341-354.


Melakeberhan H, Avendaño MF 2008. Spatio-temporal consideration of soil conditions and site-specific management of nematodes. Precis Agric 9:341-354.


Meyer, S. L. F., S. I. Massoud, D. J. Chitwood, and D. P. Roberts. 2000. Evaluation of Trichoderma virens and Burkholderia cepacia for antagonistic activity against root-knot nematode, Meloidogyne incognita. Nematology 2:871-879.


Meyer, S. L. F., D. P. Roberts, D. J. Chitwood, L. K. Carta, R. D. Lumsden, and W. Mao. 2001. Application of Burkholderia cepacia and Trichoderma virens, alone and in combinations, against Meloidogyne incognita on bell pepper. Nematropica 31:75-86.


Neher DA 1999. Nematode communities in organically and conventionally managed agricultural soils. J Nematol 31:142-154.


Neher DA 2001 Role of nematodes in soil health and their use as indicators J Nematol 33:161-168.


Neher DA 2010. Ecology of plant and free-living nematodes in natural and agricultural soil. Annu Rev Phytopathol 48:371-394.


Neher DA, Campbell CL 1994 Nematode communities and microbial biomass in soils with annual and perennial crops. Appl Soil Ecol 1:17-28.  


Neher DA, Darby BJ 2006 Computation and application of nematode community indices: General guidelines. Pages 211-222 In: Abebe, E. (editor) Freshwater Nematodes: Ecology and Taxonomy, CABI, 752 pp.


Neher DA, Peck SL, Rawlings JO, Campbell CL 1995. Measures of nematode community structure and sources of variability among and within fields. Plant Soil 170:167-181.


Neher DA, Weicht TR, Barbercheck ME 2012. Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils. Appl Soil Ecol 54:14-23.


Neher DA, Weicht TR, Bates ST, Leff JW, Fierer N 2013. Changes in bacterial and fungal communities across compost recipes, preparation methods, and composting times. PLoS ONE 10.1371/journal.pone.0079512.


Neher DA, Weicht TR, Dunseith P 2015. Compost for management of weed seeds, pathogen, and early blight on brassicas in organic farmer fields. Agroecol Sust Food Syst 39:3-18.


Noe, J. P. 1998. Crop- and nematode-management systems. Pp. 159-171. In: K. A. Barker, G. A. Pederson, and G. L. Windham, eds. Plant and nematode interactions. Agronomy Monograph No. 36. American Society of Agronomy, Madison, WI.


Nong, G., V. Chow, L.M. Schmidt , D.W. Dickson, J.F. Preston. 2007. Multiple-strand displacement and identification of SNPs as markers of genotypic variation of Pasteuria penetrans biotypes infecting root-knot nematodes. FEMS Microbiol. Ecol. 61:327-336.


Nyiraneza J 2003. Nitrogen recovery and nitrogen balance with 15N in potato systems amended with cover crops and manure. M.S. Thesis, Michigan State Univ., East Lansing.


Okada, H. & Kadota, I. 2003. Host status of 10 fungal isolates for two nematode species, Filenchus misellus and Aphelenchus avenae. Soil Biology & Biochemistry 35, 1601-1607.


Panaccione, D. G., J. B. Kotcon, C. Schardl, R. Johnson, and J. Morton. 2006. Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri, on perennial ryegrass. Nematology 8:583-590.


Paoletti, M. G., Osler GHR, Kinnear A, Black DG, Thomson LJ, Tsitsilas A, Sharley D, Judd S, Neville P, D’Inca A 2007. "Detritivores as indicators of landscape stress and soil degradation." Australian Journal of Experimental Agriculture 47(4): 412-423.


Philippot, L., Raaijmakers JM, Lernanceau P, van der Putten WH 2013. "Going back to the roots: the microbial ecology of the rhizosphere." Nat Rev Micro 11(11): 789-799.


Pretty, J.,and Bharucha, Z.P.2014.Sustainable intensification in agricultural systems. Ann.Bot. 114,1571–1596.doi:10.1093/aob/mcu205.


Pyrowolakis, A., Westphal, A., Sikora, R. A., and Becker, J. O. 2002. Identification of root-knot nematode suppressive soils.  Applied Soil Ecology 19:51-56.


Robinson, A. F., Westphal, A., Overstreet, C., Padgett, G. B., Greenberg, S. M., Wheeler, T. A., and Stetina, S. R. 2008. Detection of suppressiveness against Rotylenchulus reniformis in soil from cotton (Gossypium hirsutum) fields in Texas and Louisiana.  Journal of Nematology 40:35-38.


Schmidt, L. M., J. F. Preston, D. W. Dickson, J. D. Rice, T. W. Hewlett. 2003. Environmental quantification of Pasteuria penetrans endospores using in situ antigen extraction and immunodetection with a monoclonal antibody. FEMS Microbiol. Ecol. 44:17-26.


Schmidt, L.M., J.F. Preston, G. Nong , D. W. Dickson and H. C. Aldrich. 2004. Detection of Pasteuria penetrans infection in Meloidogyne arenaria race 1 in planta by polymerase chain reaction. FEMS Microbiol. Ecol. 48(3):457-464.


Settle DM, Fry JD, Milliken GA, Tisserat NA, Todd TC 2007. Quantifying the effects of lance nematode parasitism in creeping bentgrass. Plant Dis 91:9, 1170-1179.Sikora EJ, Guertal EA, Bowen KL (2001). Plant parasitic nematodes associated with hybrid bermudagrass and creeping bentgrass putting greens in Alabama. Nematropica 31:2, 301-306.


Siddiqui, Z. A., and I. Mahmood. 1999. Role of bacteria in the management of plant-parasitic nematodes: A review. Bioresource Technology 69: 167-179.


Sikora, R. A. 1992. Management of the antagonistic potential in agricultural ecosystems for the biological control of plant parasitic nematodes. Ann. Rev. Phytopathol. 30:245-247.


Sikora, R. A., and S. Hoffmann-Hergarten. 1993. Biological control of plant-parasitic nematodes with plant-health promoting rhizobacteria. Pp. 166-172 in R. D. Lumsden and J. L. Vaughn, eds. Pest management: Biologically based technologies. Proceedings of Beltsville Symposium XVIII. Washington, DC: American Chemical Society.


Singh, K. P., K. Bihari, and V. K. Singh. 1991a. Effect of culture filtrates of fungi colonizing neem cake on Heterodera cajani. Current Nematology 2: 9-14.


Shannon, C.E. & Weaver, W. 1949. The mathematical theory of communication. University of Illinois press, Urbana. 117pp.


Socarrás, Ana. "Mesofauna edáfica: indicador biológico de la calidad del suelo." Pastos y Forrajes 36.1 2013: 5-13.Sooby J, Landeck J, Lipson M 2007. National Organic Research Agenda, http://ofrf.org/sites/ofrf.org/files/docs/pdf/nora2007.pdf


Steel H, de la Peña E, Fonderie P, Willekens K, Borgonie G, Bert W 2010. Nematode succession during composting and the potential of the nematode community as an indicator of compost maturity. Pedobiologia 53:181–190.


Stirling, G. R. 1991. Biological control of plant-parasitic nematodes. CAB International, Wallingford, UK.Wasilewska, L. 1994. The effects of age of meadows on succession and diversity in soil nematode communities. Pedobiologia 38, 1-11.


Weibelzahl-Fulton, E., D. W. Dickson, and E. B. Whitty. 1996. Suppression of Meloidogyne incognita and M. javanica by Pasteuria penetrans in field soil. Journal of Nematology 28:43-49.


Westphal, A. 2005. Detection and description of soils with specific nematode suppressiveness. Journal of Nematology 37:121-130.


Westphal, A., Pyrowolakis, A., Sikora, R. A., and Becker, J. O. 2011. Soil Suppresivenes Against Heterodera Schachtii in California Cropping Areas. Nematropica 41:161-171.


Wick, R. L., and B. Dicklow. 2001. Occurrence of Pasteuria-infected Tylenchorhynchus in golf course putting greens. Phytopathology 91:S198.


Wickings K, Grandy AS 2013. Management intensity interacts with litter chemistry and climate to drive temporal patterns in arthropod communities during decomposition. Pedobiologia 56:105-112.


Yeates GW 1999. Effects of plants on nematode community structure. Annu Rev Phytopathol 37:127-49


Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieya SS 1993. Feeding habits in soil nematode families and genera-an outline for soil ecologists. J Nematol 25:315-331.


Zhang SH, Cao ZP, Cheng YF, Zhang G 2012 Change of soil protozoa community structure under different farming practices. J Animal and Veg Advances 11: 3140-3147.

Attachments

Land Grant Participating States/Institutions

CA, CT, FL, HI, IL, IN, MA, MI, MN, NY, OH, RI, TN, VT, WV

Non Land Grant Participating States/Institutions

USDA-ARS
Log Out ?

Are you sure you want to log out?

Press No if you want to continue work. Press Yes to logout current user.

Report a Bug
Report a Bug

Describe your bug clearly, including the steps you used to create it.