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Turfgrass

Suppressing Sting Nematodes with Brassica sp., Poinsettia, and Spotted Spurge Extracts

^a Dep. of Hortic., E-143 Poole Agric. Cent.
^b Dep. of Appl. Econ. and Stat.
^c Dep. of Entomol., Plant Pathol., Soils, and Plant Sci., Clemson Univ., Clemson, SC 29634-0319

^* Corresponding author (bmccrty{at}clemson.edu)

Received for publication August 17, 2005.

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
With synthetic nematicide options becoming limited, two studies were initiated to investigate the usefulness of selective botanical extracts for the suppression of sting (Belonolaimus longicaudatus Rau) nematodes. Plant materials were from greenhouse-grown mature specimens of spotted spurge (Chamaesyce maculata L. Small); poinsettia (Euphorbia pulcherima Willd. ‘Freedom Red’); lantana (Lantana camara var. hybrida); mature, field-grown tall lettuce (Lactuca canadensis L.); and goldenrod (Solidago altissima L. var. scabra), plus a seed meal extract from Brassica juncea ‘Pacific Gold’ (BSM). Nematodes were exposed to 1.2-mL extract of either shoot or roots of each plant species. Nematode mortality counts were made daily for 4 d. In Study 1, effects of botanical extracts on nematode mortality were evaluated when applied directly to laboratory-controlled sting nematode populations in test tubes. Root extracts of spurge, poinsettia, and lantana provided 69, 70, and 57% mortality, respectively, by 96 h while goldenrod and tall lettuce root extracts and the untreated provided 0% mortality. Shoot portions of poinsettia and spurge provided 95 to 98% mortality while goldenrod, tall lettuce, and lantana shoot extracts had 64, 40, and 25% mortality, respectively. Greenhouse studies evaluated the most successful laboratory extracts in a soil environment and included poinsettia shoot extracts and BSM. Poinsettia shoot extracts with irrigation provided 70% control compared with the untreated pots while poinsettia nonirrigated provided 73% control. Brassica sp. seed meal with irrigation provided 92% control while BSM nonirrigated provided 99.5% control. Brassica sp. seed meal, poinsettia, and spurge shoot extracts showed most promise as possible biocontrol agents of sting nematodes.

Abbreviations: BSM, Brassica sp. seed meal • DI, deionized

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
PLANT-PARASITIC NEMATODES are serious turfgrass pests, especially in warm, drought-prone environments. Sting nematodes are most problematic in sand-based rootzones such as golf greens and sports fields, especially with bermudagrass (Cynodon spp.) turf (McCarty et al., 2005). Sting nematodes are ectoparastic, feeding with their stylets penetrating into plant vascular tissue. Threshold populations for sting nematodes in warm-season grasses range from 10 to 20 per 100 cm³ of soil (McCarty et al., 2005). Above these threshold levels, sting nematodes retard overall root development, predisposing plants to moisture and heat stress.

Synthetic chemical control of nematodes is extremely limited and often inconsistent among nematode genera. Their use is restricted, including specific turf sites, rates, number of applications, and often require special equipment and special licensing to purchase and apply (McCarty et al., 2005). Repeat use of certain nematacides may also lead to enhanced microbial degradation, shortening their effective half-lives (Skipper et al., 2001).

In many sites with excessive sting nematode populations, certain plant species appear unaffected and possibly possess morphological characteristics or inherent compounds that may provide a chemical defense. Spotted spurge, a member of the Euphorbiaceae family, is often observed growing in sting-nematode-infested turf sites (McCarty et al., 2005). Spotted spurge shoots produce a milky, latex sap when pinched or disturbed, and this sap may provide a chemical defense strategy to protect itself from pest damage (Prakash and Rao, 1997). Salah et al. (1998) noted selected members of the Euphorbiaceae family possess diterpene ester-type toxins that contaminate livestock fodder and may lead to dietary cancer in humans. Since these compounds are sufficiently toxic to be considered as carcinogens in primary and secondary consumers, it appears reasonable to suspect a toxicological potential against pest infestations.

Little published information exists on the use of botanical extracts as nematicidal agents in established turfgrass. Studies evaluating the toxic effects of extracted plant materials have been limited to laboratory observations or field trials conducted on other crops. In annual crop production, cover crops and rotation schemes using nonhost plants and potentially suppressive plants have shown positive results for parasitic nematode reduction when evaluated over prolonged time periods (Crow et al., 2001). Others have shown the potential of cover crops and green manures as suppressants for nematode infection (Kinloch and Dunavin, 1993; Prot et al., 1992; Viaene and Abawi, 1998). Unfortunately, crop rotation, interplanting, and nonhost strategies are not viable options due to the perennial nature of turfgrasses.

With the limited availability of synthetic products that suppress nematodes and the apparent ability of certain plants to survive in high-nematode-infested sites, laboratory and greenhouse experiments were conducted with the objective to explore the possibility of using root and/or shoot extracts of selected plants for sting nematode biocontrol or suppression.

	MATERIALS AND METHODS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Laboratory Studies
Extract Filtration
Plant materials used for the preparation of the extract solutions were collected from mature specimens. Spurge, poinsettia, and lantana were collected from plants grown in the greenhouse while tall lettuce and goldenrod were collected from field locations near Clemson, SC. Brassica sp. seed meal was prepared from cold-pressed seed meal provided by Dr. Matthew Morra, University of Idaho.

Extracts were prepared initially using a blender and cheesecloth. Additional maceration was performed using a juice extractor and professional filtration equipment, including 0.2-µm retention pore size membranes manufactured by Millipore Corporation (Bedford, MA), Whatman International Ltd. (Maidstone, England), and Fisher Scientific (Pittsburgh, PA). The filtering process minimized the introduction of fungal hyphae, mold spores, and bacteria from harvested plants.

Root and shoot portions of each plant species were separated and compared to determine the origin of potential nematicidal compounds produced by each species. Root solutions of all plant species, along with the spurge shoot solutions, were prepared using the blender. Shoot solutions of the remaining plant species were prepared using the juicer. Brassica sp. seed meal solutions were prepared before filtration by saturating the dehydrated meal with deionized (DI) water at a 1 to 2 ratio. The solution of BSM and DI water were mixed thoroughly using a stir plate for 12 h to ensure complete saturation. Extracts were produced until 300 mL of each species were collected.

Following maceration through the blender or juicer, plant materials were pressed through layers of cheesecloth and allowed to settle in standard 500-mL beakers for 24 h. The time required for settling separated larger particulate matter from the liquid portion of the solutions, allowing microfiltration through the membranes with minimal clogging.

The filtration process was initiated using a porcelain Büchner funnel (Coors Porcelain Co., Golden, CO) with Whatman (Qualitative P5) filter paper attached to a no. 9 rubber stopper and inserted into a vacuum filtering flask. Filter flasks were utilized to hasten filtration by connecting a vacuum aspirator to a water tap. Extract solutions were poured 25 to 50 mL at a time, into the Büchner funnel and vacuumed until the filter paper was dry. Between additions of extract material to the Büchner funnel, the filter paper was changed to prevent excessive clogging and to maintain sterility.

Filtration advanced from the larger retention size filters to the smaller retention sizes using a Fisher Scientific glass microanalysis funnel. The funnel was attached to the vacuum filtering flask and contained filtration papers from 0.65-µm retention size down to 0.25 µm. The microanalysis funnel is a multipiece filtration system that includes a 300-mL borosilicate funnel, a borosilicate glass base with a 47-mm support screen (location of filter paper placement), an anodized aluminum clamp used to connect the glass base with filter paper to the container funnel during vacuum filtration, and a no. 8 perforated rubber stopper, which fits standard 1000-mL Erlenmeyer vacuum flasks.

Approximately 20 to 30 mL of prefiltered (Whatman no.5) extract solution was added at a time to the microanalysis funnel containing the 0.65-µm retention size filter paper. These methods were repeated until extracts had been filtered through the 0.45- and 0.25-µm membrane filter papers, respectively. It was hypothesized that a 0.25-µm retention-size filter paper would successfully remove most bacteria, fungi, or mold spores present on the plant material. To test this hypothesis, 3 mL of the extract solutions was pipetted into a Petri dish without a lid and exposed to laboratory atmosphere for 120 h. After 120 h, pathogen formation had not occurred, so the filtration process was deemed acceptable.

Nematode Collection
Nematode-infested soil was collected from the no. 6 fairway/rough interface at The Country Club of South Carolina in Florence, SC. Naturally infested ‘Tifway’ bermudagrass areas with histories of elevated sting nematode populations were selected at random. A pointed shovel was used to lift the turf and obtain soil samples. All soil, either attached to the bermudagrass root system or left loosely in the hole, was removed and collected in 19-L buckets with lids. The soil from each area was collected to a depth of 25 cm. Approximately 38 L of soil was collected during each golf course visit with samples being collected in adjacent sites along the fairway/rough area.

The soil was transported to Clemson University, and nematodes were extracted in the lab utilizing centrifugal flotation (Jenkins, 1964). Once separated from their soil environment, sting nematodes were carefully identified, counted, and stored in glass vials for 24 h before the experiments.

Treatment Application
Eppendorf tubes (Fisher Scientific, Pittsburgh, PA) with 1.5-mL capacity were used as the exposure environment for laboratory studies. Plant extracts (1.2 mL) were pipetted from glass storage bottles and placed into individual autoclaved eppendorf tubes. Twenty adults or juveniles (J2 stage or higher) were individually removed from the nematode suspension and placed into each tube containing the extract material. Each tube represented an individual replication for each time period.

Nematodes were exposed to plant extracts in the eppendorf tubes for 24, 48, 72, or 96 h. Eppendorf tubes with nematodes were stored in a Styrofoam tube rack at room temperature (25°C) for each individual time period. Following the specific treatment period, extract solutions with nematodes were poured from the eppendorf tube onto a 400-mesh (38-µm pores) sieve. Tubes were thoroughly rinsed onto the sieve three times, and nematodes were lightly rinsed with tap water until the extract was washed through the sieve. Nematodes were then rinsed from the sieve into 250-mL beakers and stored with 25 to 50 mL of tap water. Following a brief revitalization period (0.5 to 1 h), nematodes were poured into a 47-mm-diam. Petri dish and observed using a microscope at 10 to 63x. A fluorescent light was used as the backlight illumination source.

Nematode viability was determined by using a dentist's pulp canal file to physically stimulate a reaction from individual live nematodes. Each of the 20 nematodes in the Petri dish was lifted from the water and placed back into the water repeatedly (five times). This repetitive action caused live individuals to move their bodies in a snake-like motion when they were placed back in the water. Nematodes and plant extract were discarded following observation.

Statistical Design and Analysis
Laboratory experiments were conducted using completely randomized designs. The 12 x 4 factorial experiments consisted of all combinations of 11 plant extracts plus a water-only control and four exposure times. Two experiments were conducted in 2002—one during May–June and another in September–October. Both studies were conducted in identical laboratory environments maintained at 22°C.

Statistical analyses were performed using the SAS General Linear Models procedure (SAS Inst., Cary, NC) to evaluate main and interaction effects of the two treatment factors and to determine whether treatment effects were consistent for the two studies. Mean comparisons among plant extracts were performed using Fisher's LSD with = 0.05, and polynomial contrasts were performed to examine relationships between nematode mortality and duration of exposure to plant extracts.

Greenhouse Studies
The objectives of the greenhouse investigations were to: (i) investigate the efficacy of selected plant extracts on sting nematode control when applied to a soil environment and (ii) determine if irrigation would enhance the effectiveness of plant extracts.

Pot Establishment and Inoculation
Conetainer pots (Stuewe and Sons, Inc., Corvalis, OR) 17.8 cm in height by 3.8 cm in diameter were used in the greenhouse experiments. Common bermudagrass was seeded at 35 seeds per conetainer on the surface of a sand growth medium with particle-size distributions between 0.05 and 0.5 mm, with the largest percentage (90%) between 0.25 and 0.5 mm. The overall bulk density of the sand rootzone was between 1.3 to 1.6 g cm^–3. The sand, before seeding, was autoclaved for 15 min at 120°C and, once cooled, was used to fill the pots to 1.27 cm below the rim of the conetainer. Pots were then seeded at 35 seeds per pot, lightly watered, and covered with a plastic wrap until germination (5 d).

Following germination and growth, seedlings were clipped twice weekly at 1.91 cm. Peter's Professional (20–10–20) Water Soluble Fertilizer (Scotts-Sierra Hort Products Co., Marysville, OH) was applied to the pots according to label directions to maintain desirable growth and color for 4 wk before the investigation but was discontinued at initiation of the trials to prevent interaction with treatments.

Nematodes were extracted by the centrifugal-flotation method described before. Following extraction, nematodes were individually selected (50 adults and juveniles at a time) and placed into eppendorf tubes containing 1.2 mL of DI water. Once counted, nematodes were immediately transferred to individual pots in the greenhouse. Pots were inoculated with the nematodes using a 5-mL glass syringe, 5 d before treatment application to help stabilize and balance the study populations.

Treatment Preparation and Application
Treatment preparation via extract maceration and filtration was performed according to the methods described in laboratory studies section where the solutions were filtered through a 0.2-µm sieve. The five treatments consisted of irrigated and nonirrigated BSM and poinsettia shoot extracts plus a control.

Individual pots were treated with 15 mL of plant extract solution. Control pots received 15 mL of tap water at the same time extracts were applied to treated pots. A plastic 10-mL syringe was used to apply the treatments, 5 mL at a time, until the rootzones of the individual conetainers were saturated with plant extract solution. Each pot represented an individual treatment replication. Following treatment, irrigated pots immediately received 10 mL of tap water to ensure proper infiltration and distribution of the plant extracts into the rootzone without being excessive to facilitate leaching.

Extraction and Mortality Determination
The extraction technique was based on the methods described earlier. Briefly, following a 5-d exposure period, nematodes were extracted from individual pots in the lab using the centrifugal flotation method, and each nematode was examined for viability using the dentist's pulp canal file.

Final nematode populations (P_f) recovered from the control pots revealed 30% extraction efficiency. Extraction efficiency in these studies was based on the total number of nematodes extracted from the pots, regardless of whether the nematode was dead or alive. Mortality for the plant extract treatments, therefore, were adjusted based on the mean extraction efficiency of the control pots. The mortality rates for treated pots were calculated using the following equation (Ferris, 1987).

Statistical Design and Analysis
Due to inconsistent nematode availability during Study 1, a completely randomized design with eight replications was used. Study 2 was conducted in a randomized complete block design with eight replications blocked on application timing (date). Statistical analyses were performed using the SAS General Linear Models procedure to evaluate main and interaction effects of plant extracts and irrigation using linear contrasts with = 0.05 and to determine whether treatment effects were consistent for the repeated studies.

	RESULTS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Laboratory Studies
Results for the two laboratory studies were combined since no treatment x study interaction was detected. Significant interaction between plant extracts and duration of exposure was found, so comparisons among plant extracts were performed for each exposure time. No nematode mortality was observed for the controls throughout the laboratory studies.

Following 24 h of exposure to plant extracts, BSM was most effective and provided 99% nematode mortality while lantana and tall lettuce shoot and goldenrod root extracts were ineffective with 0% mortality (Table 1). Efficacy for the other plant extracts ranged from 20 to 50% with poinsettia shoot extract exhibiting the highest mortality within this group. After 48 h of exposure, BSM was still the most effective with 100% mortality while goldenrod root and tall lettuce shoot extracts continued to be ineffective. All other plant extracts exhibited 20 to 70% mortality with increased exposure time as evidenced by significant linear or quadratic relationships (Table 1). Poinsettia shoot extract again achieved the highest mortality within this group, but spotted spurge root and shoot extracts increased to 60% mortality.

Greenhouse Studies
The two greenhouse studies are discussed separately due to a significant treatment x study interaction for sting nematode mortality even though nematode extraction was very similar for the two experiments (Table 2). In each experiment, extraction efficiency was 29% for the controls while nematode extraction from conetainer pots receiving plant extract treatments averaged about 48% lower than the control pots. Also, a species effect was detected in each study with 50% lower nematode extraction for BSM than for poinsettia shoot extract. An irrigation effect on nematode extraction was not detected in either study.

	DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

Lantana was selected based on both field observations and historical references on the toxic nature of this species. Lantana has been observed successfully inhabiting citrus groves heavily infested with nematode populations. Morton (1971) detailed the toxic characteristics of Lantana: "Long recognized as highly toxic to grazing animals; has caused death in children when a quantity of unripe berries was eaten." Lantana produces allelopathic substances in its roots and shoots, potentially increasing its competitive ability (Smith, 1985; Sahid and Sagau, 1993). It strongly resists herbivory, contributing to its pest-plant status outside its natural range (Janzen, 1983).

Tall lettuce, a member of the Asteraceae family, was selected for evaluation due to latex sap within the aerial portions of the plant. Goldenrod, also a member of the Asteraceae family, has been historically known as a medicinal herb. Prakash and Rao (1997) listed several Solidago species as possessing insecticidal properties effective against several insects including the red-legged grasshopper (Melanoplus femmurubrum Hael) and common tulip tree aphids (Macrosiphum liriodendri Jacobson).

Lastly, BSM was selected based on Brown and Morra's (1997) research detailing the general properties of glucosinolates and the plants that produce these compounds. Their work analyzed the toxic nature of glucosinolate compounds, which when degraded, release isothiocyanate, and provided recommendations for the use of such allelopathic species for alternatives in plant pest control.

The trends from shoot evaluations were similar in both laboratory studies. The shoot portions of several selected plant species including poinsettia and spotted spurge provided more mortality than root portions of the same species. These results are similar to those previously published about many of these species dealing mainly with insect pests (Prakash and Rao, 1997). Most observations on these plants noted their pesticidal characteristics occur in the shoot and had activity against insect species.

Overall, the trends observed in the laboratory study also were observed in the greenhouse trials. Both of the selected plant species (poinsettia and BSM) provided suppression in a soil environment. If the plant extracts did not kill the nematodes, they had a noticeable effect on the general movements of the adult and juvenile populations and involved general lethargy and stiff, slow movement compared with the untreated.

The use of botanical sources as suppressants of nematode populations in important plant species has limited history. Halbrendt (1996) suggested plant compounds elicit nematode behavior such as attraction or repulsion from roots, making allelopathic research a fundamental component of nematological investigations. Halbrendt indicated naturally occurring chemicals for nematode control have advantages over the current use of synthetic chemicals, and attempts utilizing this approach have been made either by rotation, intercropping, or through the use of green manures.

Sangwan et al. (1990) studied the nematicidal activity of essential plant oils against nematodes important in vegetable production. They studied the oil constituents of several common plants species including basil (Ocimum basilicum L., family Labiatae), peppermint (Mentha piperata L., family Labiatae), kachi grass (Cymbopogon caesius Staph, family Gramineae), bottle brush (Callistemon lanceolatus DC., family Myrtaceae), tulsi (Ocimum sanctum L., family Labiatae), and dried bulbs of cloves (Eugenia caryophyllata Thunb., family Myrtaceae). Several of these oils and their constituents were active against the citrus nematode (Tylenchulus semipenetrans Cobb) while the clove oil constituent (eugenol), basil (linalool), and kachi grass (geraniol), were toxic to juveniles of seed gall nematodes (Anguina tritici Steinbuch). Furthermore, all oils except those produced by bottle brush (cineole), kachi grass (geraniol), and noneugenolic tulsi were active against the root knot nematode (Meloidagyne javonica Treub). The constituents of basil (linalool), clove (eugenol), and bottle brush (geraniol) also provided toxicity against the pigeon pea cyst nematode (Heterodera cajani Koshy).

Our study was initiated with the hypothesis several of the extracts would successfully control a nematode population with direct exposure. The lack of control with lantana or tall lettuce was somewhat unexpected as these plants grow routinely in sites of high nematode infestation. However, poinsettia and spotted spurge provided >90% reduction of the population in a controlled environment. These findings support the field observations that spurges often thrive in nematode-infested soils. Furthermore, the nematicidal effect of BSM was similar to that previously mentioned in the literature as being due to the toxic nature of the glucosinolate (or isothiocyanate) produced by the plants (Brown and Morra, 1997) although turf improvement has not always been correlated to reduced nematode populations (Crow, 2005).

Another interesting aspect of this study was that none of the root extract treatments provided adequate (90%) nematode mortality since these plants routinely are in high nematode-infested areas. Tall lettuce and lantana were slight exceptions since their root extracts had better, but still unacceptable, control of sting nematodes. Additional studies are needed on the physiology of the selected plants to better understand their strategies and specifically what compounds are involved in suppressing nematode populations. A possible explanation is that the majority of plant predators feed on the aerial portions and plants, therefore, do not need to allocate as many defensive chemicals to their root systems or these compounds are not typically in sufficient levels adjacent to plant roots.

Laboratory and greenhouse studies indicated the Brassica species that produces isothiocyanate-derived compounds from glucosinolates had a strong initial effect against the sting nematode. Plants in the Euphorbiaceae family also showed potential to cause nematode death over time, but these effects were not immediate. In nature, this is important as the concentration of the Euphorbia species plant extract may not be strong enough after 4 d, reducing its efficacy. These studies help support existing theories that certain plants in the Euphorbiaceae family may produce a compound that protects its growth in a sting-nematode-infested soil. Although this nematicidal compound may not be concentrated in the physical soil environment around the plants, the compounds within the plant prevent or reduce the nematode from feeding. The ability of poinsettia extracts to suppress nematode populations when transferred to a soil environment is unknown due to the time nematodes will require exposure.

Extract of BSM appears to have the greatest potential of the plants evaluated in this study to reduce sting nematode populations, based on the immediacy in which this extract impacted this nematode species. One potential risk of using the BSM is its phytotoxicity potential on turfgrass. Extracts of BSM, when allowed to dry on the leaf blade, caused leaf dehydration to the point of physical damage. Bermudagrass turf treated with BSM recovered within 10 to 15 d, but depending on the health of the stand before application, shoot recovery may not rapidly occur with a depleted root system from nematode feeding. Visual observations also indicated root systems appeared to remain healthy and unaffected by 5-d saturation with BSM extracts.

	CONCLUSIONS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
These studies indicate plant extracts, from members of the Euphorbiaceae family and Brassica genus, appear as potential alternatives for sting nematode suppression if the compounds can persist in the soil and plant environment for sufficient time. Plant extracts from certain plant species such as Brassica spp. are more likely to reduce a plant-parasitic nematode population in an infested soil compared with members of the Euphorbiaceae family selected for investigation in this study. Shoot extracts typically were more efficacious compared with root extracts. Lastly, irrigation appears important in the distribution of the nematicidal extract and to protect plants from phytotoxicity, especially for BSM. Future studies are needed on delivery systems of field-applied materials, specific irrigation recommendations following application, turf tolerance, and which, if any, environmental parameters influence the effectiveness of these compounds.

	ACKNOWLEDGMENTS

 
Financial support was provided by the Carolinas Golf Course Superintendents Association (CGCSA) and the Golf Course Superintendents Association of America (GCSAA). The Brassica sp. seed meal was provided by Dr. Matthew Morra, University of Idaho, and technical assistance was provided by Dr. Robin Giblin-Davis from the University of Florida, Fort Lauderdale.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Technical Contribution no.5152 of the Clemson Univ. Exp. Stn., Clemson, SC.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 

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