Nematode Management in Strawberries 1

ENY-031 Nematode Management in Strawberries 1 J. W. Noling 2 The sting nematode, Belonolaimus longicaudatus, is a pest of major importance to commercial strawberry production in Florida. Although the disease was first noticed in strawberry in 1946, it was not until 1950 that the problem was correctly identified as that of the sting nematode. The increasing importance of sting nematode on strawberry in central Florida was observed to coincide with a decrease in the use of velvet bean as a summer cover crop and an increase in the use of sesbania. During World War II, many strawberry fields which were not cover cropped, were more or less neglected and allowed to revert to native weed cover during the summer off-season. It was then observed that the extent to which a fall-planted strawberry crop was injured by sting nematode was strongly influenced by the kind of vegetation that was allowed to grow within the field during the preceding summer. The effect was so pronounced in fact, that spots of severely stunted plants could be directly related to the different, but specific, weed plants within the field during summer. A large majority of this natural weed growth was reported as crabgrass, an excellent host for sting nematode (Figure 1). Figure 1. The establishment of crabgrass (Digitaria spp.) in a cover cropped field of hairy indigo (Indigo hirsuta). Since the 1950's, B. longicaudatus has subsequently become recognized as one of the most economically important nematode crop pests in the southeastern United States, and the primary nematode parasite on strawberry in Florida. The introduction of irrigation into Florida agriculture is thought to have substantially increased cropping problems due to this nematode, especially in strawberry production. Based on evidence from other crops, parasitism by B. longicaudatus has also been shown to interact with other soilborne pests, causing a greater incidence and severity of certain fungal diseases, most notably Fusarium and Phythium. 1. This document is ENY-031 (NG031), one of a series of the Entomology & Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Published: March 1999. Revised: December 2009. For more publications related to horticulture/agriculture, please visit the EDIS Web site at http://edis.ifas.ufl.edu/. 2. J. W. Noling, professor, Entomology and Nematology Department, Citrus Research and Education Center, Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, Lake Alfred, FL 33850. The Institute of Food and Agricultural Sciences (IFAS) is an Equal Opportunity Institution authorized to provide research, educational information and other services only to individuals and institutions that function with non-discrimination with respect to race, creed, color, religion, age, disability, sex, sexual orientation, marital status, national origin, political opinions or affiliations. U.S. Department of Agriculture, Cooperative Extension Service, University of Florida, IFAS, Florida A. & M. University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Millie Ferrer-Chancy, Interim Dean

Nematode Management in Strawberries 2 The sting nematode appears to be a native pest of the sandy soils of the lower Coastal Plains of the southeastern United States. It has such a preference for sandy soils, that it fails to exist in significant numbers in soils containing even small amounts of silt, clay, or organic matter content. Sting nematode reproduction is greatest in sandy soil, at temperatures of 75-85 F (25-30 C) with constant, but moderate, moisture levels. Under suitable conditions, a life cycle is completed in about 28 days. The higher numbers and greater distribution of sting nematode in Florida is probably not only related to the predominance of fine sandy soil but also due to the warm subtropical environment. In addition, sting nematode appears to be very sensitive to sudden changes in soil conditions such as rapid drying. Figure 2. Strawberry plant stunting caused by the sting (Belonolaimus longicaudatus). Note irregular or patchy field distribution of stunted plants rather than throughout the entire field. Symptoms Strawberry production problems caused by sting nematode tend to occur in more or less definite areas where transplants fail to grow-off normally (Figure 2). Infested areas consist of spots that vary in size and shape, but the boundary between diseased and healthy plants usually is fairly well defined. Initially a field may have only a few such areas, which may then increase in size and number until the entire field becomes involved. The effect on strawberries is to cause both stunting and decline, the intensity of which is related to initial population level and the rates to which populations increase during the course of strawberry crop growth. Affected plants become semi-dormant, with little or no new growth. Leaf edges turn brown, progressing or expanding from the edges to midrib to include the entire leaf. Leaves seldom become chlorotic, although cases have been reported in which leaf yellowing occurs when essential nutrients are present in limited supply. Since the outer older leaves die first the plant gradually decreases in size and eventually may be killed (Figure 3). Sting nematode can be very damaging to nursery seedlings and transplants. As a general rule, most other crop plants are not killed unless subjected to other adverse conditions but affected strawberry plants undergo progressive decline and may eventually die. Older plants that have already developed an extensive root system can still be Figure 3. Progressive decline of strawberry due to sting nematode, Belonolaimus longicaudatus. Note death of leaves from outside in towards the crown (oldest to youngest leaves). severely affected. Under field conditions in Florida, instances are common where sting nematodes have caused only minor root system damage in the upper 3 to 4 inches of soil. In this soil zone, plants can develop a dense root system but no roots are able to penetrate below this upper layer (Figure 4). Such plants can be easily lifted or pulled from soil and are much more susceptible to droughty conditions and injury from fertilizer salt accumulations. Root growth abnormalities are caused, in part, by injury inflicted at the root tips, which results in little or no new root growth, plants lacking in fine feeder roots, and the development of short stubby branches. Root tips are killed, forcing the development of new lateral roots, whose root tips in turn are killed. This results in the production of a root system consisting of coarse roots with knobby tips. In addition, necrotic lesions may also be produced laterally along the sides of roots. Since sting nematode does not feed

Nematode Management in Strawberries 3 and overlapping glands, and males are characterized by long, pointed tails, with well developed burse. A number of physiological races have been observed based on differences in morphology and host ranges between geographic populations of sting nematode. Field Diagnosis & Sampling Figure 4. Sting nematode, Belonolaimus longicaudatus, induced symptoms on strawberry roots. Note short, dark and discolored abbreviated roots with swollen root tips. internally, the usual microscopic examination of diseased roots does not aid diagnosis since no organism is present within roots. Positive confirmation of sting nematode can only be made by soil examination. Casual Organism The original description of the genus Belonolaimus, the type species B. gracilis, and the common name 'sting' nematode was given by Steiner in 1949. Much of the early published research works in Florida strawberries reported involvement by B. gracilis. Unfortunately, only the species B. longicaudatus, described by Rau in 1958, has been reported to cause serious injury to a wide array of economically important crops, including strawberries, within the southeastern United States. Because Steiner's B. gracilis has not been observed since the original description, except for one unrecorded observation, the sting nematode associated with strawberry is now generally regarded exclusively to be that of B. longicaudatus. Morphologically, the sting nematode is identified by its unusually long, slender body (2mm) and stylet (generally in excess of 100um). Both males and females are generally numerous within the population. Females possess two ovaries, esophagus Because of their microscopic size and irregular field distribution, soil and root tissue samples are usually required to determine whether sting nematodes are causing poor crop growth or to determine the need for nematode management. For sting nematodes, sampling and management is a preplant or postharvest consideration because if a problem develops in a newly planted crop there are currently no postplant corrective measures available to rectify the problem completely once the nematode becomes established. Nematode density and distribution within a field must therefore be accurately determined before planting, guaranteeing that a representative sample is collected from the field. Advisory or Predictive Sample (Prior to Planting) Samples taken to predict the risk of sting nematode injury to a newly planted strawberry crop must be taken well in advance of planting to allow for sample analysis and treatment periods if so required. For best results, sample for nematodes at the end of the growing season, before crop destruction, when nematodes are most numerous and easiest to detect. Collect soil and root samples form 10-20 locations within the field using a cylindrical sampling tube, or if unavailable, a trowel or shovel (Figure 5). Since sting nematodes are concentrated in the crop rooting zone, samples should be collected to a soil depth of 6-10 inches. Sample in a regular pattern over the area, emphasizing removal of samples across rows rather than along rows (Figure 6). One sample should represent no more than 5 acres for such a high value crop as strawberries. Fields which have had different crops during the past season or which have obvious differences either in soil type or previous history of cropping problems should be sampled separately. Sample only when soil moisture is appropriate for working the field, avoiding extremely dry or wet soil conditions.

Nematode Management in Strawberries 4 Figure 7. Suggested strategy for collecting post-plant soil samples for nematode analysis comparing sampling results from areas of good and poor plant growth. Host Range & Damage Figure 5. The collection of soil samples for nematode analysis can be acquired from the field using either cylindrical sampling tubes, trowels, bucket auger, or shovel. Figure 6. Suggested pattern for collecting preplant soil samples for nematode analysis based on compositing soil from 10-20 field locations. For diagnostic purposes on established plants, roots and soil cores should be removed to a depth of 6-10 inches from 10-20 suspect plants. Avoid dead or dying plants, since dead or decomposing roots will often harbor few nematodes. For seedlings or young transplants, excavation of individual plants may be required to insure sufficient quantities of infested roots and soil. Submission of additional samples from adjacent areas of good growth should also be considered for comparative purposes (Figure 7). B. longicaudatus has a very wide host range including a variety of wild and commercially cultivated plants. Many different small grain and forage crops, fruits, ornamentals, and turfgrasses have all proved to be suitable hosts for sting nematode (Table 1). Most vegetable crops grown in Florida are damaged by and host the sting nematode (Table 1). Cucumber and okra are symptomless hosts but support sting nematode reproduction. Tobacco and watermelon are poor hosts, showing little or no evidence of damage in the field to sting nematode. The degree of damage expressed in the field depend upon soil population levels which in itself depends on the preceding crop or natural vegetative cover grown on the land during the summer prior to crop planting. Many weeds serve as good hosts (Table 1). Bermuda and crabgrass which have been previously implicated as native plants supporting nematode carry over during the summer and have even allowed population increase. It should be recognized that populations of B. longicaudatus collected from different areas of Florida and from different hosts may produce differing reactions to certain hosts. Differences in reaction include: 1) the plants they are capable of attacking, 2) the damage inflicted, and 3) the reproductive output of sting nematode on these crops. Based on this variability, it would be advisable to test use of these plants on a small scale against local populations to determine host status and crop susceptibility before implementing new cropping strategies on a broadscale.

Nematode Management in Strawberries 5 Control Nematode management should be viewed first and foremost as a year-round, programmatic activity requiring consideration of all cultural, chemical, and agronomic practices within the areas where strawberry plants will be grown. Because strawberry must be vegetatively propagated and transplanted into the field, growers must first pay special attention to the source of strawberry transplants to ensure they are not infested with nematodes. Growers should use only the best quality transplants available. After final harvest, the crop should be destroyed as quickly as possible to remove nematode food sources (Figure 8). In most cases, delays in crop destruction contribute to greater nematode population increase and greater difficulty in achieving nematode control. jointvetch, hairy indigo, or showy crotalaria have all been shown to reduced sting nematode populations. Hairy indigo (Indigofera hirsuta), a vigorous growing legume and excellent soil building crop has been reported to suppress sting nematode and to be resistant to several Meloidogyne spp. Velvet bean (Mucuna deeringiana), another vigorous growing legume, was also observed to suppress sting and root-knot populations in field demonstration trials. Sorghum sudangrass is a poor choice for a summer rotation on land infested with the sting nematode. Iron clay pea, widely used as a summer cover crop in the major strawberry producing areas of Florida, was recently shown to increase sting nematode populations. To be effective, cover crop stands should be established quickly and kept as free as possible of grasses and other undesirable host weeds (Figure 9). Figure 8. Use of early crop destruction as a nematode management tool in strawberry. Although specific time periods have not been quantified, field observations indicate that in the absence of a host, sting nematode will not persist in soil for a long period. Fallowing for even short durations therefore, particularly when coupled with early crop destruction, generally gives significant and immediate reduction in total nematode population densities in soil. To extend the fallow period, frequent tillage of the field may be required to maintain a clean, weed-free, fallow soil condition. The fact that soil type and soil organic matter content can also dramatically affect population levels indicates that use of soil amendments might prove useful for control. As an alternative to summer fallowing, crop rotation with a poor or nonhost crop can be another effective means for reducing soil populations of sting nematode. Cover crop rotations with american Figure 9. Rapid and extensive weed recolonization of a cover cropped field. The fact that all populations of sting nematode have such a wide host range, including numerous weeds and grasses, must be considered in developing an effective crop rotation system for nematode management. Tobacco, cucumber, okra, watermelon, and possibly peanut are the only cultivated crops which have been reported as nonhosts to some sting nematode populations. Some care should be exercised however, because most of these crops, though reported as nonhosts for the sting nematode, are excellent host for other nematodes such as

Nematode Management in Strawberries 6 Meloidogyne spp. For these rotations to be effective, weed and grass control should be as complete as possible since they can act as excellent carry-over hosts. Once again, crop rotation systems developed for a given geographical area may be of limited value in others because some local populations of sting nematode respond differently on to different hosts. In this case, small scale grower field evaluations should precede broadscale implementation of a specific crop rotation strategy. Chemical Control The sting nematode can be controlled with fumigant nematicides (Table 2 ). The use of soil fumigants for control of the sting nematode was experimentally first attempted in strawberry in 1946. From these trials it was determined that either solid fumigation treatment before bedding or row treatment as the bed were made, allowed strawberry growers to produce productive crops of strawberry on land in which sting nematode had been destructive to in previous crops. By 1964, virtually all of the Florida strawberry acreage was being treated with a fumigant nematicide which resulted in a four-fold increase in strawberry yields over that of previous nonchemical methods (Figure 10). Since 1993, when methyl bromide was added to the class I category of ozone depleting substances and a phaseout date of 2005 recently established, a considerable amount of research has been conducted by University of Florida scientists. In Florida, the principal research objective has been to identify and evaluate alternatives to methyl bromide which minimize agricultural impacts. In general, the results of these Florida studies shows that no single, equivalent replacement (chemical or nonchemical) currently exists which exactly matches the broad spectrum efficacy of methyl bromide. A summary of chemical alternatives research shows that a combination of different fumigants (1,3 Dichloropropene; Telone; and Chloropicrin; Telone C-17 or C-35 ) and a separate, but complementary herbicide treatment (Devrinol ) will be required to achieve near equivalent soilborne pest control and strawberry yield. However, in reality, it is not clear at this time whether these treatment regimes will Figure 10. Sting nematode, Belonolaimus longicaudatus, induced stunting of strawberry, comparing fumigated and nonfumigated test strips of plant row. Figure 11. Preplant soil fumigation for nematode control. survive the environmental scrutiny of our regulatory agencies or ultimately be adopted by growers due to the significantly increased needs for personnel protective equipment required for all workers in the field during application. Telone C-17 and C-35 presently requires the use of a spray suit, rubber gloves, boots, and a full face respirator by all personnel in the field at the time of application. Although efforts are underway to address both of these restrictions with the manufacturers and the U.S. E.P.A., the current label restrictions is expected

Nematode Management in Strawberries 7 to severely limit their usage in Florida strawberry production. The breadth and focus of the methyl bromide alternatives research program in Florida is not limited exclusively to evaluation of chemical combination treatment regimes. The program also encompasses an evaluation of a diversity of nonchemical tactics. Since 1993, an ever expanding list of nonchemical alternatives has been evaluated in field research and demonstration trials. Some of the nonchemical alternatives evaluated include: 1) Summer Cover Crops; 2) Pest Resistant Crop Varieties; 3) Organic Amendments; 4) Solarization; 5) Biological Control Agents; 6) Natural Product Pesticides; 7) Super Heated Water and Steam; 8) Fallowing; and 9) Paper and Plastic Mulch Technologies and Emissions Reduction. In general, the results from some of these nonchemical studies have been encouraging, but, in most cases, should be construed as incomplete from a soil pest control or crop yield enhancement perspective. Many of these nonchemical tactics are not only marginally effective (at this time) or show activity against a single target pest, but also impractical, cost prohibitive, or have requirements for specialized equipment and operators. In addition, none of the nonchemical tactics should be considered stand alone replacement strategies for methyl bromide soil fumigation at this time. As a result, new field studies evaluating combinations of tactics have been proposed or are in progress to establish cumulative impacts on soilborne pest control and crop yields. Regardless of product, effective use of any soil fumigant for nematode control requires appropriate soil preparation and conditions prior to treatment. If a fumigant is to be used, begin field preparations 6 to 8 weeks ahead of planting so that crop debris will be completely decayed (Figure 12). Since all fumigants must diffuse through soil as gases to be effective (Figure 13), the most efficient fumigations occur when the soil is well drained, in seedbed condition, and at a temperature above 60 F. Because all of the fumigants are toxic to living plants, an appropriate planting delay of 1 to 3 weeks to aerate the soil must also be observed to avoid crop injury due to phytotoxic soil residues. Figure 12. Field tillage operation as a prerequisite to soil fumigation. Figure 13. Nematode as aquatic organisms encountering both liquid and gas phase nematicides in soil. Explanation of Rates Listed in the Nematicide Table Chemicals used to control nematodes include fumigant nematicides and multipurpose fumigants. "Overall" soil fumigation is done by injecting fumigant from outlets equally spaced across the entire field. Outlets (behind chisels or coulters) are spaced: 1) All fumigants except Vapam (metham sodium): 12 inches; if less than 12 inches, the rate per outlet should be reduced proportionally. The rate of fumigant within the area actually treated should never exceed the maximum overall rate (broadcast rate).

Nematode Management in Strawberries 8 2) Vapam (metham sodium): 5 inches. "Row" application of fumigants refers to treatment of a relatively narrow band of soil with one or more outlets centered on the planting row. This generally provides adequate protection for annual crops with much less fumigant per acre of field. If two of more outlets are used per row, they should be spaced and the rate per outlet should be the same as for overall treatment. Row fumigant rates in the tables assume use of one outlet per row, with rows 36 inches apart, unless otherwise noted. Wider spacing of rows will require less total fumigant per acre, and closer spacing will require more, than the "Gal/Acre" estimate based on 36row spacing. The dosage listed for some fumigants should be increased for organic soils (peat and muck); others should not be applied to such soils; see labels. Rates of nonmaterials are given in weight or volume units of formulation. The maximum rate per 1000 ft of row should not be exceeded; wider row spacing will use less total chemical per acre, but closer row spacing must not result in more total material used per acre than the maximum permitted on a broadcast basis.

Nematode Management in Strawberries 9 Table 1. Host status to sting nematode, Belonolaimus longicaudatus, to various turf, forage fruit, vegetable, and agronomic crops. Good Hosts Poor or Nonhost Turf, Field and Forage Crops Bluegrass Bentgrass Centipedegrass St. Augustine Bahia Bermuda Pangola grass Fescue Corn Oats Millet Rye Wheat Peanut* Clovers Cotton Soybean Barley Lespedeza Tobacco Fruit and Vegetable Crops Beans Carrots Celery Sweet corn Cowpea Eggplant Onion* Pea Citrus* Strawberry* Cabbage* Cantaloupe Cauliflower Endive Lettuce Tomato Turnip Eggplant Okra* Cucumber* Snapbean Squash Pepper Sweet potato* Potato Watermelon* Asparagus Hot pepper Cover Crops Sesbania Sorghum/Sudan grass Iron Clay pea Crabgrass Bermuda Fescues All members of grass family Mungbean Pigeonpea Lambsquarter* Cudweed Dogfennel Johnsongrass Common Weeds Hairy vetch Joint vetch Beggarweed Ragweed Wild carrot Spanish needle *Variable host response to geographic/physiologic races of sting nematode. Hairy Indigo Crotalaria Velvet bean* Bidens Horseweed Buckhorn plantain Pokeweed Sandbur Cocklebur* Jimson weed Sorrel Wild garlic Jerusalem oak Table 2. Fumigant nematicides for strawberries in Florida. Broadcast Application 1 Nematicide Gallons or Lbs Per acre Fl oz /1000 ft / chisel spaced 12" apart In the Row Applications Methyl Bromide Chloropicrin A critical use exemption (CUE) for continuing use of methyl bromide for Florida Strawberry has been awarded for calendar years 2009 and 2010. Specific certified uses and labeling requirements for CUE acquired methyl bromide must be satisfied prior to grower purchase and use in these crops. Quantity and formulation availability are subject to change.

Nematode Management in Strawberries 10 Table 2. Fumigant nematicides for strawberries in Florida. Broadcast Application 1 Nematicide Gallons or Lbs Per acre Fl oz /1000 ft / chisel spaced 12" apart In the Row Applications Telone II 2,3 27 to 35 gal 79 to 102 For any row spacing, application rates given may be concentrated in the row, but shall never exceed the labeled maximum for broadcast applications. Consult the product label for additional detail. Telone C-17 2,3 32.4 to 42 gal 95 to 123 For any row spacing, application rates given may be concentrated in the row, but shall never exceed the labeled maximum for broadcast applications. Consult the product label for additional detail. Telone C-35 2,3 39 to 50 gal 114 to 146 For any row spacing, application rates given may be concentrated in the row, but shall never exceed labeled maximum for broadcast applications. Consult the product label for additional detail. Telone InLine 2,3 29 to 56 gal - For drip fumigation, consult the product label for overall rate, drip concentration and flow modifying application directions. Pic Chlor 60 2,3 19.5-31.5 gal 57 to 90 Consult product label for overall rate and chisel flow modifying application directions. Pic Chlor 60 EC 2,3 19.5-31.5 gal - For drip fumigation, consult product label for proportionately reduced overall rates, drip concentration and drip flow modifying directions and procedures. Midas 98:2 2,4 Midas 50:50 2,4 100-175 lb (5.3 9.3 gal) 150-350 lb (9.4 22 gal) - Compared to broadcast application, apply proportionately less for in the row applications based on the ratio of bed width to row spacing. Consult the product label for additional detail and rate modifying recommendation. - Compared to broadcast application, apply proportionately less for in the row applications based on the ratio of bed width to row spacing. Consult the product label for additional detail and rate modifying recommendation. Vapam HL 75 gal - For drip fumigation and crop termination, consult product label for proportionately reduced overall rates, drip concentration and flow modifying directions and procedures. KPam HL 60 gal - For drip fumigation and crop termination, consult product label for proportionately reduced overall rates, drip concentration and flow modifying directions.

Nematode Management in Strawberries 11 Table 2. Fumigant nematicides for strawberries in Florida. Broadcast Application 1 Nematicide Gallons or Lbs Per acre Fl oz /1000 ft / chisel spaced 12" apart In the Row Applications 1 Gallons/acre and fl oz/1000 feet provided only for mineral soils. Higher rates may be possible for heavier textured (loam, silt, clay) or highly organic soils. 2 All of the fumigants mentioned are for retail sale and use only by state certified applicators or persons under their direct supervision. New supplemental labeling for the Telone products must be in the hands of the user at the time of application. See label details for additional use restrictions based on soil characteristics, buffer zones, requirements for Personal Protective Equipment (PPE) and rate modifying recommendations with use of highly retentive mulch films. 3 Higher application rates are possible in the presence of cyst-forming nematodes. 4 Midas 98:2 and 50:50 for Tomatoes, Pepper and Strawberry only. Certification required for application. Rates are believed to be correct for products named, and similar products of other brand names, when applied to mineral soils. Higher rates are required for muck (organic) soils. However, the grower has the final responsibility to see that each product is used legally; read the label of the product to be sure that you are using it properly.