Coastal northern California is home to several of America’s top 100 golf courses, including Cypress Point Club, Pebble Beach Golf Links, The Olympic Club, San Francisco Golf Club, Spyglass Hill Golf Course, and Monterey Peninsula Country Club (Shore and Dunes Courses) (Whitten, 2019). All of these golf courses, and many more along the coast from Carmel to Mendocino, have been affected at one time or another by pacific shoot-gall nematode (Anguina pacificae), which was first discovered in 1978 (Costello, 1983). Identified initially as Anguina radicicola, Cid Del Prado and Maggenti (1984) renamed the nematode with its current name. An endoparasitic pathogen of annual bluegrass (Poa annua), it is damaging primarily to putting greens. It infects host shoots at the base of the crown. Symptomatic galls soon develop, containing any combination of eggs, adults, and juveniles (McClure et al., 2008). Usually two, but as many as four, generations can occur in 1 year. Second-stage juveniles (J2) can be infective to new shoots most of the year. A moisture film is essential for nematode dissemination outside the galls. The J2 move from the soil onto the young shoot surface and toward the crown (Giat et al., 2008). Usually, infection happens from spring to late fall during warmer temperatures (50 to 70 °F) and wet or foggy weather. Symptoms progress from small, yellow to brown patches that enlarge to cause a rough, uneven surface that could result in a complete turf loss (Giat et al., 2008; McClure et al., 2008).
Several golf courses affected by pacific shoot-gall disease resorted to regrassing their greens to creeping bentgrass (Agrostis stolonifera), which is considered not susceptible to the nematode, even though McClure et al. (2008) noted minor production of shoot-galls in some creeping bentgrass cultivars. More concerning is that annual bluegrass is a ubiquitous species that is well adapted to coastal climates like northern California. Without effective and selective means of controlling annual bluegrass in creeping bentgrass greens, the species quickly reinfests putting surfaces and becomes prone to pacific shoot-gall nematode-caused infection.
Plant protection against pacific shoot-gall disease has been challenging because of the lack of effective and safe nematicides. Historically, fenamiphos was the last nematicide used against this nematode, even though over time, its efficacy diminished. Eventually, the U.S. registration was withdrawn in 2008 (McClure and Schmitt, 2012). The nematicide became also the focus of regulatory action in other countries (Australian Pesticides and Veterinary Medicines Authority, 2015). As a replacement, many golf course superintendents in California resorted to using products containing azadirachtin as the active ingredient. It is a mixture of triterpenoids extracted from seeds of the neem tree (Azadirachta indica). Azadirachtin and by-products of the neem tree have long been used as a treatment against certain fungi and insect pests as well as human diseases (Khalil, 2013). Mode of action in insects includes disruption of critical pathways needed for growth, molting, and chemoreceptors, leading to antifeeding effects [Aerts and Mordue (Luntz), 1997; Khalil, 2013; McClure et al., 2008]. McClure and Schmitt (2012) identified azadirachtin in a growth chamber bioassay as one treatment with the potential to disrupt the life cycle of pacific shoot-gall nematode. No nematodes were found in galls 60 d after treatment, and the authors hypothesized that azadirachtin either induced juveniles to stop feeding or arrested their development. Azadirachtin is environmentally safe and breaks down readily under field conditions; thus, frequent applications are usually required for efficacy (Khalil, 2013). It was suggested that it should be applied on a biweekly basis throughout the growing season, which for California means from March to November or longer (McClure and Schmitt, 2012).
Fluopyram is a pyridinyl-ethyl-benzamide compound belonging to the succinate dehydrogenase inhibitor (SDHI) group of fungicides [Fungicide Resistance Action Committee (FRAC, 2020) Code No. 7] with broad-spectrum efficacy against all the stages of fungal growth. Its activity includes, but is not limited to, Ascomycetes, such as gray mold Botrytis, Sclerotinia, and Monilinia species, on various crops (Veloukas and Karaoglanidis 2012). More recently, fluopyram was discovered to possess nematicidal properties (Fürsch et al., 2015). It was initially registered in cotton (Gossypium sp.) and soybean (Glycine max) as a seed- and soil-applied nematicide, often combined with the insecticide imidacloprid (Velum Total; Bayer CropScience, Research Triangle Park, NC). Fluopyram was effective against various species of plant-parasitic and free-living nematodes (Beeman and Tylka, 2018; Faske and Hurd, 2015) but caused some phytotoxicity in soybean (Kandel et al., 2016). In southern root-knot nematode (Meloidogyne incognita) infested field trials with fresh market carrot (Daucus carota), fluopyram achieved good protection efficacy but only to the shallow depth of mechanical incorporation (Becker et al., 2019). In soil column experiments, limited downward mobility was influenced by soil type and application method (Faske and Brown, 2019).
The objectives of this research were to test fluopyram for efficacy against pacific shoot-gall disease on annual bluegrass putting greens in northern California, including rates and application frequency, compared with azadirachtin. The surveys included monitoring populations of other frequently occurring plant-feeding nematodes, such as spiral (Helicotylenchus spp.), ring (Criconemella spp.), and root-knot (Meloidogyne spp.), nematodes.
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