1) SUMMARY
The sugarbeet-cyst nematode (SBCN) Heterodera schachtii and/or root-knot nematode (RKN) Meloidogyne spp. occur in many sugarbeet fields in California and cause significant yield losses. Historically, the use of l,3-Dichloropropene (Telone II®), a B2 carcinogen, has been the nematicide of choice. Following the suspension of Telone II® in California (April 1990), a study was conducted by SRI International to assess the influence of the suspension on agricultural production in California. Accordingly, SRI International estimated that because Telone II® was not available, increased yield losses in sugarbeets due to nematodes in 1991 vs. historic average losses was $6.1 million, and that increases in other nematicide treatment costs in sugarbeets was $16 million (Landels, 1992). Renewed use of Telone II® in California has only recently been approved, and on a very limited scale.
The first recorded nematode pathogen of sugarbeets was SBCN, and it remains a primary pathogen throughout California (Altman & Thomason, 1971; Cooke, 1993; Roberts and Thomason, 1981). SBCN is common and is a significant problem in most areas of the world where sugarbeets are grown (Potter and Olthof, 1993). The SBCN has hosts in a range of plant families, approximately 200 hosts in 98 genera from 23 of 49 families investigated by Steele (1965). Of the agronomic crops that are known hosts, most occur within the Chenopodiaceae (sugarbeet, fodder beet, red beet, mangolds, and spinach) and the Cruciferae (cabbage, kale, Brussels sprouts, broccoli, cauliflower, turnip, kohlrabi, mustard, and radish)
In 1978, more than 200,000 acres in California were reported infested with the SBCN (Roberts and Thomason, 1981). SBCN is thought to have been brought into California many years ago and to have been accidentally distributed throughout much of the older sugarbeet growing areas. It is not prevalent north of Yolo and Sacramento Counties or in the Tulare, Kings, and Kern growing areas. Elsewhere, it is considered the major nematode problem on sugarbeets. Several species of RKN are widely distributed throughout all sugarbeet growing areas, and the nematode is known to cause damage in most. In all regions other than the Tulelake Basin, populations consist primarily of four species, with some species containing several races: M. incognita, M. hapla, M. javanica and M. arenaria (Siddiqui et al., 1973). Approximately 80 percent of the time that identifications are made, M. incognita is present. The remainder of identified RKN are divided among the other three species. It is possible for mixed populations of RKN species to occur in a single field. In the Tulelake Basin, populations of RKN are predominately M. chitwoodi but also include M. naasi and M. hapla. Sugarbeets are a new crop for the Tulelake Basin. They are known hosts for the RKN species present, but major losses have not yet been attributed to those nematodes.
The RKN and SBCN are considered, respectively, to be the first and third most important plant-parasitic nematode in the world (Eisenback and Triantaphyllou, 1991; Sasser and Freckman, 1987). Because of its importance on sugarbeets, considerable research on SBCN has been conducted in California (Baldwin and Mundo-Ocampo, 1991; Caswell and Thomason, 1991; Gardner and Caswell-Chen, 1993, 1995; Lear et al., 1966; Roberts, 1985; Roberts and Thomason, 1981; Roberts et al., 1980; Steele, 1984).
Historically, both crop rotation and nematicides have been used to control SBCN (Altman and Thomason, 1971; Cooke, 1993) while RKN control has been mainly via chemical nematicides. Typically for SBCN, rotations of three years or longer are required to reduce SBCN populations to levels below the damage threshold. Rotations in Northern California appear to be less successful than in southern growing areas, with rotations of eight to 10 years being necessary in many instances. It is suspected that this is, at least partially, due to poor weed management during rotations. This extended rotation period results in relatively few acres being available each year for sugarbeet production. Consequences for the industry have been severe in recent years because each processing plant needs to draw from a minimum number of acres to operate efficiently.
Nematodes are microscopic roundworms with a life cycle consisting of an egg, four juvenile (J) stages, and the sexually mature adult stage. In SBCN, the second-stage infective juvenile (J2) hatches from the egg, is attracted to host roots by exudates, penetrates a host root, and establishes a permanent feeding site. The nematode feeds and grows to the adult stage, with the adult female retaining most of the eggs (up to 600) internally. The female body hardens after death, protecting the eggs from adverse environmental conditions (Roberts and Thomason, 1981). Activity, reproduction, and development occur between 8-35º C, and reproduction is most rapid between 21-27º C (Thomason and Fife, 1962; Caswell and Thomason, 1991). The developmental periods from J2 to J3, J4, adult, and the next generation J2 have been found to be 100, 140, 225 and 399 degree-days (base 8º C), respectively (Griffin, 1988, Caswell and Thomason, 1991). Cysts containing eggs persist in soil for many years in the absence of a host. Although the presence of host roots stimulates egg hatch, a certain number of eggs hatch each year, even in the absence of a host resulting in a slow decrease in viable eggs.
For RKN, the invasive J2 hatches from the egg and seeks a feeding site within a root (Roberts and Thomason, 1981). The juvenile molts to the J3 and begins enlarging as the reproductive system develops. Nematodes that become females are no longer mobile, and are unable to leave the root. They continue to enlarge as they go through the J3 and J4 stages. During this time, cells around the head of the nematode enlarge to form nurse cells or giant cells. For RKN, galls will typically develop on the root. Upon becoming adults, RKN will begin to lay eggs (up to several hundred) which are contained in a gelatinous matrix at the posterior end of the body. The egg mass may be within the root or partly or wholly exposed on the root surface while the swollen body of the female remains within the root. Adult males are rare in RKN and not required for reproduction. In SBCN, males are more common and are required for reproduction. It has been shown that males become more plentiful when food sources are limited.
Temperature is also an important factor in the development of species of RKN. In those RKN species studied, approximately 600 degree days are required per generation. However, the minimum temperature for infection and reproduction vary considerably between species, which affects the overall length of time per generation and number of generations per growing season in different areas of the state. For example, the minimum temperatures for infection by M. chitwoodi, M. hapla, and M. incognita are 6, 12, and 18º C, respectively. The minimum levels for reproduction are 6, 12, and 10? C, respectively.
2) CURRENT PEST MANAGEMENT PRACTICES
Nematode management options include: nematicides, growing nematode- resistant cultivars, growing nonhost primary crops (rotations), growing nonhost cover crops, using fallow periods, enhancing natural biological control, and implementing cultural practices (Thomason and Caswell, 1987).
Chemical Controls: The following chemicals are registered for nematode management in sugarbeets: l,3-dichloropropene (Telone II®), aldicarb (Temik®), chloropicrin, metam-sodium (e.g. Vapam®) and DiTera (a toxin produced by a fungus).
Cultural Controls: Relatively unsophisticated rotation to nonhost crops is the major cultural practice in use for SBCN management. For SBCN this includes crops other than cole crops and mustard. The species of RKN found throughout the major sugarbeet growing areas have very broad host ranges. Nematode resistant processing tomatoes containing the Mi gene would be a typical nonhost rotation crop for several species. At the present time, biological control and mechanical methods are not utilized in nematode management on sugarbeets.
Effective Nematode Management: Effective nematode management requires combinations of tactics, and the tactics are selected relative to the nematode species, crop possibilities, environmental conditions at a given location, and potential economic impact. For example, if a nematicide is registered for a given crop the grower may decide to use it, if it is effective against the nematode in question and an (often intuitive) economic cost-benefit analysis is positive. Alternatively, the use of cultivars resistant to the main nematode species in a field is often effective. Frequently, however, there are several damaging species present, and cultivars with resistance to multiple nematode species are not available. In addition, nematode species differ in their host ranges, and plants differ in their host status to various nematodes. These differences are the basis for crop rotation sequences. After defining what nematodes are present in their fields, growers may consult nematological "experts" to reach a management decision. Even the "experts" have a difficult time constructing a decision given the volume of information that should be considered. Because of this, at the present time, there is little integration among the various control methodologies. Development of a knowledge-based system is needed to make integration a reality.
3) REDUCED-RISK OPTIONS
Because of the complex nature of nematode management, a number of management
approaches are needed including: development of a knowledge-based system,
development of damage thresholds, evaluating the effectiveness of reduced
risk nematicides against SBCN and RKN, and developing management techniques
for deployment of SBCN-resistant sugarbeet cultivars (which are being developed
by other researchers).
(A) Evaluate the effectiveness of reduced risk nematicides
against SBCN and RKN: The potential for the loss of methyl bromide
and other soil fumigants has stimulated the development of new nematicides
by a number of companies. Based on the data developed, the first
"biological" nematicide, DiTera, was recently registered on sugarbeets
in California. This is the first new nematicide to be registered
on sugarbeets since aldicarb (Temik®) was registered more than 30 years
ago. Even though this product is registered, additional testing is
needed to determine how to best integrate its use into the sugarbeet cropping
system. For example, there is evidence that it can be utilized synergistically
in combination with carbamates such as Temik® with greatly reduced
rates of both products. Other companies with promising products include
Zeneca and Mycogen (a fatty acid nematicide).
Ozone gas is another promising candidate. In the laboratory, ozone movement through several soil types at different moisture levels has been evaluated in terms of mass transfer of ozone and nematode survival. For SBCN, soil containing cysts was treated at 380 and 1,890 kg/ha with ozone generated from air and from oxygen. Hatch of larvae from eggs was reduced, with a greater reduction at the higher rates. In a second trial, soil at 3.3 and 6.7 percent moisture were treated with ozone generated from air at 158 and 6700 kg/ha. At both moisture levels, the higher rate reduced subsequent hatch of eggs. For RKN, soil at two moisture levels (four and eight percent) was treated at 380 and 1,890 kg/ha onzone generated from air or from oxygen. All treatments reduced RKN larvae. Field trials have been conducted against RKN on carrots and on tomatoes in which ozone gas was injected at 246 kg/ha through buried drip irrigation tubing. On both crops, significant nematode reductions were demonstrated, and for tomatoes, yields were increased compared to the untreated. These new products need to be evaluated in comparative trials with currently registered products.
(B) Develop resistance-management techniques for SBCN on resistant sugarbeets: The genetic variability of different California populations of SBCN, what that variation means in terms of damage caused by nematodes, and the potential for resistance-breaking races of SBCN needs to be assessed. Previous research supported by the California Beet Growers Association and USDA-NRI has revealed that much genetic variability exists in California SBCN (Caswell-Chen, Westerdahl).
In general, populations of the cyst nematodes (as a group) are known to be genetically variable. Resistant cultivars have been developed in other crops to manage some of the cyst nematode species parasitizing those crops. Genetic variability is common in species of the Heteroderidae. Pathotypes, or races, are defined by nematode compatibility with resistance genes (Riggs and Schmitt, 1988). Pathotypes of the potato-cyst nematode able to reproduce on potatoes carrying single dominant genes for resistance have been identified (Stone, 1985). Pathotype shifts occurs due to directional selection pressure that occurs with resistance deployment, and directional selection via soybean and barley resistance genes has resulted in the recognition of 16 H. glycines pathotypes (Riggs and Schmitt, 1988) and 10 H. avenae pathotypes (Sidhu & Webster, 1981), respectively. It has been suggested that as new sources of resistance are deployed, new cyst nematode pathotypes are selected (Hartwig, 1981; McCann et al., 1989). Available evidence indicates that SBCN pathotypes exist (Graney & Miller, 1980; Griffin, 1981; Lear & Miyagawa, 1972; Muller, 1992; Steele, 1975, 1984). If SBCN is to be managed through resistance or crop rotations, genetic variation within and among populations must be characterized (Caswell & Roberts, 1987; Opperman et al., 1994).
Different California populations of SBCN show different genotypes as measured by random amplification of polymorphic DNA. Genetic diversity exists among SBCN populations in California (Caswell-Chen et al., 1992). The influence of such variation relative to aggressiveness and virulence on different hosts is not fully understood. Experiments with European cultivars have recently been conducted on SBCN-resistant oilseed radish to determine the efficacy of such plants against California SBCN (Caswell-Chen, Westerdahl). Experiments in California SBCN reveal that selection by the oilseed radish does result in SBCN capable of parasitizing the resistant plants. This raises a "caution" flag regarding the eventual deployment of resistant sugarbeets in California.
Although the development of SBCN-resistant sugarbeets has been slowed
by the difficult genetics of sugarbeets, recent developments will expedite
the development of such cultivars. In the past it has been difficult
to do experiments with SBCN on "resistant" beets, because only about 75
percent of a seed lot would actually carry resistance. The recent
identification and cloning of the SBCN resistance gene from a wild sugarbeet
relative will allow identification of plants carrying resistance by using
molecular markers (using RAPD and AFLPs), so a program can now be embarked
upon to assess how widespread resistance-breaking SBCN is in California.
This will be quite valuable information, prior to deploying the resistance
in the field, as other researchers are currently developing commercial
sugarbeet cultivars resistant to SBCN. This will allow us to develop,
based on estimates of selection, rotation schemes to allow effective deployment
of resistance for some time to come.
(C) Development of a user-friendly, knowledge-based ("expert")
system: This will be a computer-based aid for sugarbeet growers and
processors in making nematode management decisions, specifically regarding
nematicide application, and crop and cultivar selection which will be available
via the Internet and World Wide Web (WWW).
Scientific progress, with attendant proliferation of reductionist knowledge has led to overwhelming amounts of information and a proliferation of informational databases (e.g., Blake and Bult, 1996; Caswell-Chen et al., 1995; Eeckman and Durbin, 1995; Ferris et al., 1995; Lyons, 1990; Shoman et al., 1995). Although the reductionist research strategy is highly effective in generating information, it does not directly lead to access, organization, integration, and interpretation of information, the vital components that allow application of knowledge in practical, real-world problem-solving activities (Schmoldt and Rauscher, 1996). There is a critical need to be able to access and interpret knowledge on nematode management. Access to information via the WWW only assists in implementation because access to informational databases is only one component necessary for application of knowledge.
Nematode management relies on the synthesis of a range of information for informed decisions (Thomason and Caswell, 1987), and effective management strategies potentially involve the manipulation of multiple system attributes to achieve management objectives. In the case of nematode management in sugarbeets, all the components mentioned above need to be available for effective decision making.
A semantic network approach in the development of the knowledge-based
system (Lucas and van der Gaag, 1991; Schmoldt and Rauscher, 1996) has
been initiated. The user will provide input to the system, including:
the nematode species, the nematode density, the crop from which soil samples
were taken, the desired crops for the next three years, willingness to
use nematicides (yes or no), soil type, geographic location (user will
also be able to note nearest location to specific cities), and priorities
of management objectives (improving yield, growing high value crop, prefer
short-term or longer-term benefits, and reducing nematode population increase).
The information needed to develop such a system as described above already exists. As additional data are developed as described herein, they will be incorporated into the knowledge-based system to permit more sophisticated predictions.
(D) Development of damage thresholds: Development of damage thresholds for SBCN and RKN will increase the number of acres available each year for planting sugarbeets, will permit growers to utilize nematicides only when justified by expected economic returns, and holds promise for rapidly minimizing reduction of nematicide use in this cropping system.
Nematode management in annual crops can be based on the fact that there is typically an inverse relationship between the numbers of nematodes and crop yield (e.g. Seinhorst, 1965). A critical-point, quantitative functional relationship between nematode population density at planting and relative crop yield was established for annual crops by Seinhorst (1965) as:
where
M = the minimum relative yield in the presence of high
nematode densities,
T = the initial nematode density at which relative yield
is reduced, or the tolerance limit,
Z = a term for the per capita damage to plant roots, considered
the proportion of the root system that remains undamaged by a single nematode;
typically a value slightly less than one,
P = the initial (preplanting) nematode density (also,
Pi)
This quantitative relationship has proved useful for defining
the damage caused by various nematode densities (Ferris, 1986), and for
different nematode species and crops (Ferris, et al., 1986), including
SBCN (Cooke, 1991) and RKN. Once established for a particular crop-nematode
interaction in a particular environment, it allows nematode management
decisions to be based on the crop loss (Y) given the nematode densities
(P) in the field.
Establishing a good fit between the Seinhorst function and field data is sometimes difficult because of field variation (Ferris, 1984b). A successful approach will be used to addressing such variation by subdividing the initial population densities into nematode density classes and solving the Seinhorst functional relationship as described by Ferris (1984b). This approach allows the establishment of damage function confidence intervals. Yield functions will be converted to an economic basis using commodity prices as seasonally available and untreated and treated plots compared relative to nematode density.
Damage thresholds for SBCN have been developed for the Imperial Valley growing area (Roberts and Thomason, 1981). During the past few years, with funding from the C.B.G.A. and the UC IPM Project and cooperation from the sugarbeet industry, a number of fields with SBCN in the San Joaquin and Sacramento Valley growing region have been extensively sampled, and a data set has been produced which will be analyzed to develop damage thresholds and optimum methods for sampling commercial sugarbeet fields to determine damage thresholds for SBCN.
Each field was divided into a grid of small plots and intensively sampled to define the initial nematode density (Ferris, 1984a). Because nematodes are not uniformly distributed throughout a field, each plot contains different nematode densities, and plots range from very low levels (zero to near zero) to levels that are sufficiently high to reach minimum yield. Nematode samples (initial and final populations, Pi and Pf, respectively) and harvest samples were collected from each plot. Nematode populations were assessed using standard extraction methods (Roberts and Thomason, 1981; Caswell et al., 1985).
Fields were planted, cultivated, and harvested following standard commercial practices. Yields were obtained from each plot to establish a data set of paired data for initial populations and yields. Relative yields are defined by establishing the maximum, or 100 percent, yield as the highest yield obtained from the field, with remaining yields described as fractions of the maximum. Thus, the standardized, observed maximum yield takes implicit account of yield variation among different field locations. After the relative yields from the plots are calculated, the Seinhorst function is fit by regression (Draper and Smith, 1981) to the paired data for each field and the threshold estimated (Ferris, 1984b). This analysis will be conducted for individual fields and then for grouped fields to detect variation among locations. The importance of variation among field locations will be assessed via multivariate approaches (multiple regression, canonical correlation, and discriminant function analysis) that also incorporates environmental parameters (specifically temperature) to help determine those fields that will be particularly susceptible to crop loss due to nematodes (Afifi and Clark, 1990).
Soil temperature data from the UC IPM IMPACT computer system for the CIMIS station closest to each field will be used. Soil physical characteristics per field have been analyzed by the UCD CE Soils Diagnostic Lab. Correlation between damage and soil type will be assessed during data analysis.
Trials will be established to develop damage thresholds for RKN on sugarbeets. Initially, these will be conducted in a field at the University of California South Coast Research and Extension Center infested with RKN (M. javanica). Prior to the planting of sugarbeets, a grid (three feet by 20 feet) of 100 plots will be established in the field and 100 soil samples will be taken to establish initial population densities. Sugarbeets from each plot will be harvested, weighed, and analyzed for sugar yield (with industry cooperation). A damage threshold will be developed from the data as described above. Trials in growers' fields will be conducted as opportunities are identified.
4) CHALLENGES
Because of the stringent nature of the Food Quality Protection Act (FQPA), replacement pest management systems are badly needed for the sugarbeet industry. Historically, a B2 carcinogen, l,3-dichloropropene (Telone II®), has been the most widely used nematicide in sugarbeet production. The second most widely used nematicide has been the carbamate aldicarb (Temik®). The use of Telone II® in California was suspended for several years because of human exposure to nematicides due to off-site movement in the air. Although its use has been reinstated, it is under constant evaluation, has increased significantly in cost, and could be suspended again at anytime if detected in the air above California--even at parts per trillion levels. If for any reason (such as FQPA evaluation) Telone II® and Temik® become unavailable, growers are left with only three registered products: metham-sodium, chloropicrin, and DiTera. None of these products has been tested extensively enough on sugarbeets to allow prediction of efficacious methods of application. In addition, both metham-sodium and chloropicrin pose significant hazards for human exposure due to off-site movement.
5) INNOVATIVE FEATURES IN REDUCED-RISK PROGRAM
This evaluation is innovative in several ways. If successful
in evaluating the potential for resistance-breaking isolates of SBCN in
California prior to the widespread deployment of SBCN-resistant beet germplasm,
it will be a first in the annals of nematode management via resistance.
In the past, when crops resistant to other species of cyst nematode have
been developed, their useful life has been short because methods to incorporate
them into management programs have not been developed so as to avoid the
selection of resistance-breaking nematode strains. Successive cropping
to the same variety has selected for resistance-breaking strains of nematodes
within a very few years. Information on resistance management developed
in this evaluation will be incorporated into the knowledge-based system
(the next topic) so that the most effective way to manage resistant varieties
of sugarbeets can be utilized by growers in conjunction with other management
techniques.
This proposal is innovative from another perspective. At the present time, user-friendly, knowledge-based ("expert") systems available via the Internet and World Wide Web (WWW) are not available for any California crop. The problems with nematicide use are well known, and any way to decrease their use is environmentally beneficial. However, the traditional nematicides have provided effective and consistent control with a single recommendation effective statewide. Reduced-risk products and methods will not have this same benefit. Individualized programs will need to be developed for each field dependent on its geographical location and the particular nematode species present. Utilizing the knowledge-based system which will incorporate the damage thresholds to be developed in conjunction with soil temperature information available from CIMIS stations, together with information to be developed on reduced-risk nematicides, will allow the development of individualized nematode-management programs that are economically, environmentally, and socially acceptable. Development of damage thresholds will reduce the pesticide load in the environment. They will allow growers to decide whether or not nematode populations warrant a nematicide treatment relative to a particular field and a particular planting date. The availability of economic/damage thresholds will reveal that population levels in many fields are below the economic/damage threshold, too low to justify nematicide application. This will increase the predictability and thereby the effectiveness of pest-control techniques. Growers frequently use nematicides without clear demonstration that the costs are justified. As nematode damage potential is temperature dependent, it is likely that some applications during the cooler months are not needed. The data obtained will delineate times of the year when temperatures are too low for growers to obtain an economic return from nematicide application.
6) BARRIERS TO ADOPTION OF REDUCED-RISK METHODS
Cost is the major barrier to adoption of any new management method on
sugarbeets. This is a relatively low value crop in California and
growers have limited resources. This is a major reason why the development
of a knowledge-based expert system available over the WWW to assist with
economic evaluation of alternatives will be invaluable to the industry.
This research will have significant impacts on the obvious and the hidden
costs of sugarbeet production. The obvious impact will result from
reducing nematicide applications and hence costs. After this research
is completed, the actual savings realized can be estimated by comparing
pesticide use records (from the UCIPM IMPACT Computer System), before and
after the project. Some of the nematicide-cost savings will be replaced
by nematode sampling costs, approximately five dollars per acre, required
for nematode sampling and analysis. Traditional crop production economics
tend to underestimate the true total costs for nematicide use because they
do not include the cost of pesticides on the environment (e.g. water and
air pollution, farm worker health and safety, and impacts on nontarget
organisms). Such "hidden" savings will likely be much greater than
the economically obvious savings. Regulations should not be a hindrance
to the adoption of the reduced-risk methods to be developed. The
nematicides to be evaluated are either already available for use in the
state (DiTera and ozone) or sufficiently environmentally friendly that
registration should be achievable. Social concerns should be alleviated
rather than exacerbated by the proposed plan. The proposed plan is
designed to overcome currently existing information gaps and technical
issues. The sugarbeet industry is well-organized, with extensive networks
for education already in place linking the AES researchers, farm advisors,
specialists, growers, industry, PCAs, and the USDA-ARS.
REFERENCES
Afifi, A. A., and V. Clark. 1990. Computer-aided multivariate analysis. New York: Chapman and Hall. pp. 505.
Altman, J., and I. J. Thomason. 1971. Nematodes and their control. In: Johnson, R. T., J. T. Alexander, G. E. Rush, and G. R. Hawkes (eds.), Advances in Sugarbeet Production: Principles and Practices. Ames, IA: Iowa State University Press. pp. 335-370.
Baldwin, J. G., and M. Mundo-Ocampo. 1991. Heteroderinae, cyst-and non-cyst forming nematodes. IN: W. R. Nickle, ed. Manual of agricultural nematology. New York: Marcel Dekker. pp. 275-362.
Caswell, E. P., I. J. Thomason, and H. E. McKinney. 1985. Extraction of cysts and eggs of Heterodera schachtii from soil with an assessment of extraction efficiency. Journal of Nematology. 17:337-340
Caswell, E. P., and P. A. Roberts. 1988. Nematode population genetics. In: J. A. Veech and D. W. Dickson, eds. Vistas on nematology. Maryland: Society of Nematologists. pp. 390-397.
Caswell, E. P., and I. J. Thomason. 1991. A model of egg production by Heterodera schachtii (Nematoda: Heteroderidae). Canadian Journal of zoology. 69:2085-2088.
Caswell-Chen, E. P., V. M. Williamson, and F. F. Wu. 1992. Random amplified polymorphic DNA analysis of Heterodera cruciferae and H. schachtii populations. Journal of Nematology. 24: 343-351.
Caswell-Chen, E. P., H. Ferris, B. B. Westerdahl, and R. L. Sloan. 1995. A PC/MAC -platform database on the host status of crop and weed species to plant-parasitic nematodes. Nematology Newsletter: An official publication of the Society of Nematologists. 41(2): 7-8.
Cooke, D. A. 1991. The effect of beet cyst nematode, Heterodera schachtii, on the yield of sugarbeet in organic soils. Annals of Applied Biology. 118:153-160.
Cooke, D. 1993. Nematode parasites of sugarbeet. In: Evans, K., D. L. Trudgill, and J. M. Webster (eds.), Plant Parasitic Nematodes in Temperate Agriculture. London: CAB International. pp. 133-169.
Draper, N.; and H. Smith. 1981. Applied regression analysis. New York: Wiley and Sons. Eeckman, F. H., and R. Durbin. 1995. ACeDB and Macace. In: H. F. Epstein and D. C. Shakes (eds), Caenorhabditis elegans: Modern biological analysis of an organism, Methods in Cell Biology 48:583-605.
Eisenback, J. R., and H. H. Triantaphyllou. 1991. Root-knot nematodes. Meloidogyne species and races. IN: Nickle, W. R. (Ed.). Manual of Agricultural Nematology. New York: Marcel Dekker. pp. 191-274.
Ferris, H. 1984a. Probability range in damage predictions as related to sampling decisions. Journal of Nematology. 16:246-251.
Ferris, H. 1984b. Nematode damage functions: The problems of experimental and sampling error. Journal of Nematology. 16:1-9
Ferris, H. 1986. Nematode population dynamics and management. IN: Leonard, K. J., and W. E. Fry (Eds.), Plant Disease Epidemiology. New York: MacMillan. pp. 180-204.
Ferris, H., D. A. Ball, L. W. Beem, and L. A. Gudmundson. 1986. Using nematode count data in crop management decisions. California Agriculture. 40:12-14.
Ferris, H., E. P. Caswell-Chen, and R. L. Sloan. 1995. Synopsis of a developing database on the host status of plants to nematodes. Journal of Nematology
Gardner, J., and E. P. Caswell-Chen. 1995. Influence of cyst maturation on apparent population increases by Heterodera schachtii on root remnants. Accepted for Publication: Fundamantal and Applied Nematology
Gardner, J., and E. P. Caswell-Chen. 1993. Penetration, development, and reproduction of Heterodera schachtii on Fagopyron esculentum, Phacelia tanacetifolia, Raphanus sativa, Sinapis alba, and Brassica oleracea. Journal of Nematology. 695-702.
Griffin, G. D. 1988. Factors affecting the biology and pathogenicity of Heterodera schachtii on sugar beet. Journal of Nematology. 20: 396-404
Hartwig, E. E. 1981. Breeding productive soybean cultivars resistant to the soybean cyst nematode for the southern United States. Plant Disease 65:303-307.
Landels, S. P. 1992. Assessment of economic impacts on growers of Telone' 5 unavailability in California and information base for market reentry. SRI International, Health and Performance Chemicals Center, Palo Alto, California. SRI Project 3242. 287 pages.
Lear, B., S. T. Miyagawa, D. E. Johnson, and C. B. Atlee, Jr. 1966. The sugar beet nematode associated with reduced yields of cauliflower and other vegetable crops. Plant Disease Reporter. 50:611-612.
Lucas, P., and L. Van der Gaag. 1991. Principles of expert systems. Reading, MA: Addison-Wesley. pp. 518.
Lyons, J. M. 1990. Database of alternatives to targeted pesticides. Report to the Vice President's Task Force on Pest Control Alternatives.
McCann, J., V. D. Luedders, and V. H. Dropkin. 1982. Selection and reproduction of soybean cyst nematodes on resistant soybeans. Crop Sci. 22:78-80.
Muller, J. 1992. Detection of pathotypes by assessing the virulence of Heterodera schachtii populations. Nematologica 38:50-64.
Opperman, C. H., K. Dong, S. Chang. 1994. Genetic analysis of the soybean -Heterodera glycines interaction. In: F. Lamberti, C. DeGeorgi, and D. McK. Bird (eds.), Advances in Molecular Plant Nematology. pp. 65-75.
Riggs, R. D., and D. P. Schmitt. 1988. Complete characterization of the race scheme for Heterodera glycines. J. Nematol. 20:392-395.
Schmoldt, D. L., and H. M. Rauscher. 1996. Building knowledge-based
systems for natural resource management. New
York: Chapman and Hall. pp. 386.
Roberts, P. A. 1985. Nematodes. IN: Integrated pest management for cole crops and lettuce. University of California Statewide Integrated Pest Management Project Division of Agriculture and Natural Resources. Oakland. Publication 3307
Roberts, P. A., and I. J. Thomason. 1981. Sugarbeet pest management: Nematodes. Division of Agricultural Sciences, University of California, Special Publication 3272, 30 pp.
Roberts, P. A., I. J. Thomason, and H. E. McKinney. 1980. Influence of nonh~sts, crucifers, and fungal parasites on field populations of Heterodera schachtii. Journal of Nematology. 13:164-171.
Sasser, J. N., and D. W. Freckman. 1987. A world perspective on Nematology: The role of the society. IN: J. A. Veech and D. W. Dickson, (Eds.) Vistas on Nematology. Maryland: Society of Nematologists, Inc. pp. 7-14.
Seinhorst, J. W. 1965. The relation between nematode density and damage to plants. Nematologica 11:137-154.
Shoman, L. M., E. Grossman, K. Powell, C. Jamison, and B. R. Schatz. 1995. The worm community system, Release 2.0 (WCSr2). In: H. F. Epstein and D. C. Shakes (eds), Caenorhabditis elega~s: Modern biological analysis of an organism, Methods in Cell Biology 48:607-625.
Siddiqui, I. A., S. A. Sher, and A. M. French. 1973. Distribution of plant parasitic nematodes in California. State of California Department of Food and Agriculture Division of Plant Industry. 324 pages.
Sidhu, G. S., and J. M. Webster. 1981. The genetics of plant-nematode parasitic systems. Bot. Rev. 47:387-419.
Steele, A. E. 1965. The host range of the sugarbeet nematode, Heterodera schachtii, Schmidt. Journal of the American Society of Sugarbeet Technologists 13:573-603.
Steele, A. E. 1975. Population dynamics of Heterodera schachtii on tomato and sugarbeet. J. Nematol. 7:105-111.
Steele, Arnold E. 1984. Nematode parasites of sugar beet. IN: Plant and Insect Nematodes. W. R. Nickle, (Ed.) Marcel Dekker, Inc. pp. 507-568.
Stone, A. R. 1985. Co-evolution of potato cyst nematodes and their hosts: Implications for pathotypes and resistance. Bull. O.E.P.P. 15:131-137.
Thomason, I. J., and E. P. Caswell. 1987. Principles of nematode control. In:R. H. Brown and B. R. Kerry, (Eds.), Principles and practice of nematode control in crops. Academic Press. Pp. 87-130.
Thomason, I. J. and D. Fife. 1962. The effect of temperature on development and survival of Heterodera schachtii. Nematologica. 17: 139-145.
Nematodes contributed by E. P. Caswell-Chen, PhD. and Becky Westerdahl,
PhD., Nematology, University of California, Davis.