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Biology and Management ofNematodes on Turfgrass inNorthern CaliforniaA variety of microscopic roundworms lurking just beneaththe surface poses a challenge for putting surfaces.BY B. B. WESTERDAHL, M. A. HARlVANDi , AND L. R. COSTELLO

N ematode damage on Poaannua putting greens has beena recurring problem on

Northern California golf courses.Nematodes typically found causingdamage to turf include: root knot(Meloidogyne sp.), ring (Mesocriconemasp.), dagger (Xiphinema sp.), lesion(Pratylenchus sp.), stubby root (Tri-chodorus sp.), pin (Paratylenchus sp.), andsting nematode (Belonolaimus longi-caudatus). In addition, we have recoveredlarge numbers of spiral nematode (Heli-cotyknchus sp.) from problem turfgrasslocations.

In 1982, from San Francisco, SanMateo, and Monterey counties ofCalifornia, Anguina pacificae, a seed andleaf gall nematode, was first identifiedfrom Poa annua galls located at the basesof stems. Since this finding, A. pacificaehas been considered to be the primarynematode causing problems on coastalgolf courses in Northern California.

The organophosphate nematicideNemacur (fenamiphos) has been usedin the management of A. pacificaeand other nematodes on turfgrass inCalifornia (Winterlm et al, 1986).Recently, the nematode problem hasbecome increasingly more noticeableboth on courses that have used Nema-cur and on those that have not. Nema-cur will be withdrawn from the marketin the near future, and replacementmanagement techniques are needed.

Up to this point, the life cycle of A.pacificae has not been completely under-

Anguina pacificae lives within these galls visibleat the base of the plant.

stood. To further the development ofenvironmentally sensitive programs fornematode management, a survey wasconducted to determine the distribu-tion of A. pacificae and other nematodeson coastal golf courses in Northern

California. Following the survey, twogolf courses were selected for biweeklymonitoring of nematode populations.Additionally, a trial comparing theeffectiveness of six potential products asreplacements for Nemacur was con-ducted on a golf course green inNorthern California.

SETTING UP THE TRIALSTo survey for nematodes, one or morecores were taken with a cup cutter fromat least one green on 14 golf courses inMonterey, San Francisco, and SanMateo counties (Table 1). Galls wereindividually removed from the coresand dissected.

Following the survey, a single greenwas selected at the Olympic Club GolfCourse in San Mateo County and

Table 1Populations of various nematodes found on golf courses in Northern California.

Nematodes Per Liter of Soil

Golf Course

BayonetCypress PointDel MonteLake MercedMonterey PeninsulaNorthwood

Olympic ClubPacific GrovePebble BeachPoppy HillsPresidioQuail LodgeSan FranciscoSpyglass

Spiral

6,20022,500

9,60013,26090,240

5,7606,857

3,6004,200

12,9009,2009,6004,114

600

Ring

504,200

38,40010

1 2,0009,1201,6001,800

33,0001,800

027,9002,2291,350

Root-Knot

150300650

00

1,45029,400

050

1,20000

35050

S E P T E M B E R - O C T O B E R 2 0 0 5

Table 2Number of Anguina galls and nematode populations within galls following nematicide applications.

Treatment Rate/Acre Galls Females

Untreated 13.0 13.3Nemacur IOG 66.7 Ib/A 2.8 0.09 2.5 0.02DiteraDF 100 Ib/A 17.3 0.77 14.0 0.68A- 1641 20lb/ IK 11.8 1.00 8.0 0.74A- 1641 I5LB/ IK 17.0 0.67 16.5 0.56Quillaja35% 1.5 GPA 12.8 0.72 4.3 0.17Quillaja35% 2.5 GPA 16.5 0.97 7.5 0.27XRM 5053 3 GPA 14.5 0.78 15.0 0.66Fore 28 liters 25.7 0.41 20.5 0.40Fosthiazate 3 Ib AI/A 1.5 0.03 0.5 0.01

Each figure is the mean of 4 replicates.

ImmatureMales Adults

8.51.3 0.038.8 0.984.3 0.446.5 0.731.8 0.105.0 0.223.8 0.25

14.0 0.800.0 0.01

19.012.38.0

15.07.8

17.513.010.812.84.8

0.130.340.740.110.690.640.080.350.01

Juveniles

105.50.5

12.51.3

123.312.0

1.0124.062.5

238.5

0.350.740.460.900.620.400.890.720.51

Eggs

1,745.363.0

1,422.32,486.3

902.3940.0

1,697.82,554.52,700.5

0.0

0.010.010.200.290.460.710.990.980.67

TotalAdults

40.816.030.827.330.823.525.529.547.3

5.3

0.010.640.580.750.090.470.700.730.01

TotalNematodes

146.316.543.328.5

154.035.526.5

153.5109.8243.8

0.030.550.390.920.330.350.920.920.21

Each mean is followed by the probability that it is statistically different from the untreated.

Rate indicates amount of product applied for each of 3 applications at 4- to 6-week intervals.

Galls indicates galls counted per inch of soil core.

Other figures are total counts per 1 0 galls per replicate.

Total adults is the sum of females plus males plus immature adults.

Total nematodes is the sum of total adults plus juveniles.

another at Poppy Hills Golf Course inMonterey County to monitor thepopulation cycling of the four nema-todes found most commonly duringthe survey. Three cup-cutter cores weretaken biweekly from each green.Nematodes were extracted from soilaround roots and were identified togenus and counted under a dissectingmicroscope.

For the management trial, a greenat the Olympic Club that was heavilyinfested with A. padjicae, spiral nema-tode, ring nematode, and root-knotnematode was selected. The treatmentswere: untreated, Nemacur IOG (Bayer),DiTera DF (Valent), two rates of A-1641(mustard bran, Uniroyal/Crompton),two rates of Quillaja 35% (DesertKing), XRM 5053 (1,3-dichloropropeneplus emulsifier, DowAgro Sciences), andFore (mancozeb, Dupont) (Table 2).Applications were followed by 0.5 inchof irrigation via overhead sprinklers.During the trial, the green was main-tained by the course following standardcultural practices.

Each treatment was applied a total ofthree times at 4- to 6-week intervals.Turf quality was evaluated and nema-tode samples were taken 6 weeks fol-lowing the final application. Applica-tions were conducted on September

30, October 30, and December 12,2003. Nematode samples were taken onJanuary 20,2004.

Nematodes were extracted from soilaround roots and the number of gallsper inch of surface area was counted.Ten galls were individually removedfrom the cores and dissected under adissecting microscope. From each dis-sected gall, the number of adult malesand females, immature adults, juveniles,and eggs was determined.

Turf quality was visually determinedby the golf course superintendent basedon standards acceptable for that location.Digital photos were taken from a slopeoverlooking the plot and a representa-tive photo in which all replicates werevisible in full sun was selected for digitalanalysis of turf quality. The digitalanalysis was conducted with the histo-gram function of Adobe Photoshop setfor RGB analysis.

RESULTS AND DISCUSSIONA.padjicae was found on Poa annuagreens in all golf courses (12) surveyedin Monterey, San Francisco, and SanMateo counties (Table 1). For twoadditional courses with bentgrass greens(Lake Merced and Presidio), A.padjicaewas not found on the greens but waspresent in surrounding areas. In addi-

tion, all courses surveyed had abundantpopulations of spiral nematode, 13 hadring nematode, and 9 had root-knotnematode. Other nematodes foundoccasionally and in lower populationswere: needle (Longidorus sp.), pin(Paratylenchus sp.), stubby root (Tricho-dorus sp.), sheath (Hemicydiophora sp.),lesion (Pratylenchus sp.), and cyst (Hetero-dera sp.).These findings indicate thatalthough A.padjicae is widespread incoastal Northern California golfcourses, there is potential for othernematodes to be causing problemsas well.

When sampled at 2- to 6-inch incre-ments, nematodes were abundant at alldepths (data not shown).This indicatesthat although the galls of A.padjicae arelocated close to the surface, methods tokill populations of other nematodeswill need to be effective to greaterdepths. Although they were not alive,A.padjicae, spiral, and ring nematodeswere recovered from a water sampletaken from a pipe draining a green,indicating the ability of nematodes tomove in drainage systems.

Two of the nematodes, A.padjicaeand root-knot, monitored in the bi-weekly survey are endoparasitic nema-todes. Juvenile nematodes penetrateplant tissues, and the adults mature and

G R E E N S E C T I O N R E C O R D

OLYMPIC CLUB10,000

9,000

8,000

7,000

6,000

5,000

4,000

3,000

2,000

1,000

Figure I

ANGUINA JUVENILES ,PER QUART OF SOIL {

POPPY HILLS000

6,000

; 5,000

4,000

3,000

2,000

1,000

0 50 100 150 200 250JAN MAR MAY JUL SEP

300 350 400NOV DEC

In the nematode management trial,by visual observation, it was evidentthat turfgrass quality in Nemacur- andfosthiazate-treated plots was superior toall other treatments. Some improvementin quality was visible in the DiTera-treated plots compared to the untreated,while the remaining treatments couldnot be visibly distinguished from theuntreated. The digital photographanalysis conducted using the histogramfunction of Adobe Photoshop supportedthe visual analysis (data not shown). Thered analysis indicated that Nemacur andfosthiazate treatments were superior tothe untreated. Of the products tested,only Nemacur 10G, DiTera DF, andFore are currently registered for use onturf in California.

Several treatments reduced popula-tions of A. pacificae (Table 2). Nemacurreduced the number of males, females,

lay eggs within the plant. The datareported are for populations ofjuveniles found within soil aroundroots. These are the populations mostlikely to be affected by nematicideapplications. Spiral and ring nematodesare ectoparasites of turf, always beingfound outside of roots in the soil.

Populations of all four nematodesfluctuated throughout the year. Pvingnematode populations were consider-ably higher at the Olympic Club thanat Poppy Hills. Populations at theOlympic Club were highest inSeptember, and at Poppy Hills inNovember. As with ring nematodes,populations of root-knot nematodeswere typically higher at the OlympicClub than at Poppy Hills, with peakpopulations occurring in April andSeptember. Peak populations of root-knot nematodes at Poppy Hills werereached in September and November.Levels of spiral nematodes were similarat both locations, with the highestpopulations occurring at the OlympicClub in mid-August and at Poppy Hillsin early November. Populations of A.pacificae peaked in June at Poppy Hillsand in August at the Olympic Club.

Population sampling for nematodes was conducted by Dr. Becky Westerdahl at several coursesin the San Francisco and Monterey Bay areas.

S E P T E M B E R - O C T O B E R 2 0 0 5

Damage to a Poa annua golf course green caused by the nematode Anguina padficae.

eggs, total adults, and total nematodes.Fosthiazate reduced the number ofgalls, females, males, immature adults,and total adults. DiTera reduced thenumber of eggs. None of the treatmentsreduced populations of root-knot,spiral, or ring nematodes (data notshown). For several treatments, popula-tions of spiral nematodes were signifi-cantly higher than for the untreated.Increased nematode populations couldoccur if the treatments permitted thedevelopment of a healthier root systemthat could sustain higher populations ofnematodes. This was also the case forone treatment with ring nematodes.

LITERATURE CITEDAyoub, S. M. 1977. Plant nematology: Anagricultural training aid. Sacramento, Calif.

California Department of Food and Agriculture,Division of Plant Industry.

Byrd, D.W.Jr., K. R. Barker, H. Ferris, C.J.Nusbaum, W. E. Griffin, R. H. Small, and C. A.Stone. 1976. Two semi-automatic elutriators forextracting nematodes and certain fungi fromsoil. Journal of Nematology 8:206-212.

Cid del Prado Vera, I., and Maggenti, A. R. 1984.A new gall-forming species of Anguina Scopoli,1777 (Nemata: Anguinidae) on bluegrass, Poaannua L., from the Coast of California Journalof Nematology 16:386-392.

RadewaldJ. D, and B. B. Westerdahl. 1988.Nematode Diseases of Turfgrass. In TurfgrassPests. University of California, Division ofAgricultural Sciences Publication 4053.

Westerdahl, B. B., E. Caswell-Chen, andJ. Hartin. 2000. Nematodes. In Turfgrass PestManagement Guidelines. In U.C. Pest Manage-ment Guidelines, IPM Education and Publica-tions (eds.). University of California, Agricultureand Natural Resources Publication 3339,Oakland, Calif.

Winterlin, W, F. Peterson, and L. R. Costello.1986. Nemacur residue in turfgrass. CaliforniaAgriculture 40(1 & 2).

ACKNOWLEDGMENTS: Funding wasprovided by the USGA, NCGA, severalNorthern California golf courses, and theUniversity of California SlossonFoundation. The cooperation of the golfcourses mentioned, the NCGA, and theUSGA was essential to the success of thisresearch.

B. B. WESTERDAHL, Extension Nematolo-gist/Professor of Nematology, University ofCalifornia, Davis, Calif. M. A. HARIVANDI,University of California Cooperative Exten-sion, Alameda, Calif. L. R. COSTELLO,University of California CooperativeExtension, Half-Moon Bay, Calif.

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