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From the July 2017 issue of GCM magazine:

New golf course nematicides

New nematicides are filling the gap left in the toolboxes of superintendents who relied on Nemacur, but a single product will likely not be sufficient to replace the old standby.

Cup cutter samples were collected in Florida in May 2017
from Tifdwarf bermudagrass infested with sting
and root-knot nematodes. The sample on the left
was treated with Indemnify nematicide in summer 2016,
and the one on the right was not treated.
Photos by W.T. Crow

William T. (Billy) Crow, Ph.D.; J. Ole Becker, Ph.D.; and James H. Baird, Ph.D.

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The past two decades have brought major shifts in pesticides — in general and in turfgrass nematicides specifically — because of the implementation of the Food Quality Protection Act of 1996. We have moved away from reliance on a single effective nematicide (Nemacur), through a period without potent nematicide options (4), and into a time where several novel turfgrass nematicides are or will be available. The past two years have seen the launch of three new turfgrass nematicides in most states: Divanem from Syngenta, Indemnify from Bayer, and Nimitz Pro G from Quali-Pro. These three nematicides along with several others released since 2010 provide multiple weapons in the arsenal against nematodes. However, for many, the question remains: Do these new nematicides work as well as Nemacur? To answer this, we need to review a little about Nemacur, the types of nematodes that damage turf, and preliminary research data on the effectiveness of these new nematicides. We will then evaluate the properties of Divanem, Indemnify and Nimitz Pro G, and their relative efficacy on the four nematode genera that are currently the most problematic on golf course turf in the United States: sting, lance, root-knot and Pacific shoot-gall nematodes.

The active ingredient in Nemacur was fenamiphos, an organophosphate pesticide that affects the nervous system. Because all nematodes have similar nervous systems, they were all impacted by Nemacur. Further, fenamiphos has both contact and systemic activity and, therefore, is effective on nematodes in soil and, to some degree, inside roots. Nemacur was a very versatile treatment; it worked well against all turfgrass nematodes (10). The new nematicides can work just as well as Nemacur — and in some cases better — but not across the board on all the different species of nematodes.

Major turf nematodes

Sting nematodes

Sting nematodes (Belonolaimus and Ibipora species) are strict ectoparasites. They feed on plant roots while remaining in the soil. All the life stages of sting nematode (eggs, juveniles and adults) reside in the soil. Consequently, they can be killed by either contact nematicides through direct exposure, or by systemic nematicides that they ingest while feeding. University of Florida research has shown that during cooler months (fall through spring in Florida), these nematodes are generally active in the top 4 inches (10 cm) of the soil profile. However, during the hot summer months, sting nematodes move deeper in the soil, and many will be 6 inches (15 cm) or deeper at that time (5). For best control of sting nematode, a nematicide needs to move through the thatch and into the soil underneath. 

Lance nematodes

A bermudagrass green in Florida infested by sting nematode in spring. The center area was treated with Indemnify the previous fall, and the areas to the left and right were not treated.

Lance nematodes (Hoplolaimus species) are migratory endoparasites, meaning that they move into, move out of, and burrow within roots. At any given time, some lance nematodes will be in the soil, and others will be inside of roots (8). Systemic nematicides are more effective on this type of nematode. Contact nematicides can be very effective on the lance nematodes in the soil, but those inside roots will be unaffected until they exit the root. Therefore, to effectively control lance nematode, a nematicide’s contact active ingredient needs either to stay in the soil for a long time or to be applied frequently so that nematodes leaving roots get exposed to it over time.

Root-knot nematodes

Root-knot nematodes (Meloidogyne species) are sedentary endoparasites. They enter a root, move to the central cylinder where they establish a feeding site, and remain there for the rest of their life. Eggs are deposited into an egg mass either inside the root or at the root surface. The second-stage juvenile hatches from the egg and enters a root near its root tip. The root-knot nematode is thus potentially exposed to contact nematicides for only a short part of its life cycle. Systemic nematicides work best on these nematodes because they may affect all the life stages of the nematode within the root. Contact nematicides only impact root-knot nematodes if eggs are exposed at the root surface, or during the short period the juveniles are outside the root. Research at the University of Florida has found that the most common root-knot nematode species on turf in that state (Meloidogyne graminis) proliferates in roots growing in the thatch and upper 1.5 inches (3.8 cm) of soil (5). Therefore, a contact nematicide will be most effective if the active ingredient remains in the thatch and upper soil and then either stays there a long time, or there are repeated applications over time. Nematode numbers decline over time as multiple generations of nematode juveniles exit the roots and get exposed to the nematicide.

Pacific shoot-gall nematodes

Pacific shoot-gall nematodes (Anguina pacificae) are primarily endoparasites; only the second-stage juveniles occur outside plant tissues. They have a very limited host and distribution range. For all practical purposes, they occur only on annual bluegrass (Poa annua) in coastal Northern California. In contrast to the previously mentioned species, these nematodes feed on aboveground plant tissues (9). Infective juveniles need a thin water film to move from the soil up the surface of a young shoot to its tip. There, they penetrate the plant tissues and induce a cavity-containing gall that develops at the base of the grass shoot. Inside the cavity, the nematodes molt twice and develop into adults. Sexual reproduction is required for fertile offspring. The next generation hatches from the eggs, but it requires decomposition of the galls and perhaps their destruction by mowing for the juveniles to be released. Again, a water film is necessary for the juveniles to move to the next shoot tip or into the soil. Nemacur used to be the only nematicide registered in California that provided superintendents with useful activity against Pacific shoot-gall disease. Its efficacy seemed to decrease, however, during the years just before it was withdrawn from the market.

New nematicides

Divanem

Abamectin is the active ingredient in Syngenta’s new turf nematicide Divanem. Abamectin is not new chemistry; in fact, it has been a common active ingredient in insecticides and miticides for decades. The nematicidal properties of abamectin have also been long recognized. It is closely related to ivermectin, used to rid nematode parasites from animals and people. Abamectin is broadly effective on all kinds of nematodes and will kill any kind of nematode it contacts at very low concentrations. Despite this, abamectin has only recently been adopted for nematode management, mostly because of its major limitation: It does not move well in soil. Its water solubility is very low, while the soil adsorption value for abamectin is extremely high. It binds rapidly to organic matter and clay minerals. When sprayed onto the turf surface and irrigated, very little abamectin makes it through thatch. Abamectin has excellent contact activity on nematodes, but it is not systemic. The half-life in soil is about two weeks to a month. Abamectin is rapidly broken down in sunlight, so it should be watered-in immediately after application. Divanem has the same active ingredient as Avid, a Syngenta insecticide that was labeled for use against nematodes on greens in several states a few years ago. However, the Divanem formulation is specifically designed for application to soil, which makes it an improvement over Avid for management of turfgrass nematodes.

Bermudagrass field plots at the University of Florida severely infested with root-knot nematode. Arrows indicate the two plots that were treated with Divanem.

Root-knot nematodes tend to proliferate in the thatch and upper 1.5 inches of soil. This is exactly where most of the active ingredient in Divanem stays. In Florida, this makes Divanem an excellent product for management of root-knot nematodes on greens. As the juvenile nematodes exit the root, they are exposed to abamectin and die. About the time the abamectin starts to break down, another application needs to be made. Successive generations of nematodes are therefore impacted over time.

Sting, lance and other nematodes occurring in the upper soil profile also are affected by abamectin, but timing can be important. Just before breaking dormancy in the spring, bermudagrass will slough off many of the previous year’s roots. At that time, a much higher percentage of lance nematodes are in the soil and exposed to contact nematicides. Therefore, initiating the Divanem application sequence before spring green-up will increase the chance of success in controlling lance nematodes. Because sting nematodes move higher up in the soil profile during the cooler months, applications made during that time will be more effective than applications made in the heat of summer. Interestingly, University of Florida research has found that ring nematodes (Mesocriconema ornatum) move up in the soil profile during summer, so summer applications will work better for those nematodes. 

In Florida, the best results with Divanem have been from four applications of the maximum labeled rate (12.2 fluid ounces/acre [0.89 liter/hectare]) at four-week intervals. It is important to go through the entire sequence, because one or two applications are usually not sufficient to give the desired results. Other ways to improve efficacy of Divanem are to tank-mix it with a good soil penetrant and apply it following aerification. At the University of Florida, we have had much improved turf responses from Divanem when it was combined with a good fungicide program. In California, Divanem became available for research purposes in late 2016. Our preliminary results indicate that the product appears to have a positive effect on the recovery of Poa annua turf from Anguina damage at high rates and monthly intervals. However, plant-parasitic nematode populations in soil as well as Anguina, root-knot, ring and spiral nematodes were not affected.

Indemnify

The active ingredient in Bayer’s new nematicide Indemnify is fluopyram, which is also an SDHI (succinate dehydrogenase inhibitor) fungicide. In Florida, we have evaluated other commercially available SDHIs and have not found them to be nematicidal like fluopyram. The soil adsorption value of fluopyram is intermediate — although some of the active ingredient will bind to the thatch, plenty of it makes it through to kill nematodes in the soil. One of the unique properties of fluopyram is that it has an extremely long soil half-life of six months to two years. This means that Indemnify can provide longer nematode suppression than other turf nematicides. Fluopyram is a contact nematicide, although it is taken up by roots and moved upward through xylem to control foliar diseases caused by fungi. As an SDHI fungicide, Indemnify should be considered a FRAC Group 7 fungicide for resistance management. 

Nimitz Pro G being applied to a golf green. The newer nematicides are safer for both people and the environment, and professional applicators are required to wear only minimal personal protective equipment when they apply either Nimitz or Indemnify, which are both labeled “Caution,” indicating the lowest hazard level.

Research at the University of Florida has shown Indemnify to have broad activity on most types of nematodes. It has proved effective on sting, root-knot, ring nematodes, etc., in lab and field trials. However, labeled rates of Indemnify are not effective on lance nematodes. Because of its intermediate adsorption value, enough of it gets bound up in thatch to provide good results on root-knot nematode. It will move out of thatch slowly over time, so root-knot nematode control starts to diminish a couple of months after the last application. Sting and other plant-parasitic nematodes in the soil will be impacted as the fluopyram moves through the thatch and into the soil below. In University of Florida trials, Indemnify provided reductions in sting nematode numbers and positive turf responses for six to eight months or longer after the last application. If root-knot nematodes are the primary target, irrigate only lightly after application. For sting nematodes, irrigate with ¼ inch (0.6 cm) of water to help move the fluopyram through the thatch.

Researchers from the University of California, Riverside conducted a number of trials with Indemnify against the Pacific shoot-gall nematode on golf courses from the coastal Monterey Peninsula to the San Francisco Bay Area. At extremely low rates of 0.195 or 0.39 ounce/1,000 square feet (5.95 or 11.9 grams/100 square meters), one to two applications provided season-long protection of annual bluegrass on putting greens that had heavy infestations of Anguina pacificae. The nematicide had little or no effect on soil-dwelling root-knot, ring or spiral nematode populations. We hypothesize that the long persistence of fluopyram continuously protects new growth of Poa annua against shoot infections and, consequently, gall formation. This breaks the life cycle and eventually leads to Anguina population reduction in the soil.

Nimitz Pro G

Quali-Pro’s Nimitz Pro G is a granular formulation of fluensulfone, a new chemistry in its own chemical class. Fluensulfone has both contact and systemic activity, so it can kill nematodes in soil and perhaps within turf roots. It has a low adsorption value; in Florida, it moves readily through thatch and into the soil below. The half-life is relatively short, so multiple applications of lower rates tend to work better than one or two applications of higher rates. For golf courses, either four applications of 60 pounds/acre (67.25 kilograms/hectare) or three applications of 80 pounds/acre (89.66 kilograms/hectare) at monthly intervals have yielded the best results. In contrast, in cool, coastal California, Nimitz Pro G had no effect on Pacific shoot-gall disease. Soil populations of A. pacificae as well as those of ring or spiral nematodes were unchanged compared with the non-treated control.

A putting green suffering from an infestation of Anguina pacificae, which is found in coastal areas of Northern California. Corners of three plots are marked by golf balls: left plot, untreated; center plot, treated with Divanem;
right plot, treated with Indemnify.
Photo by James Baird

In Florida, fluensulfone has shown activity against sting, lance and root-knot nematodes in lab and field trials. Because it has systemic activity, it can be effective on lance and root-knot nematodes inside of roots in addition to nematodes present in the soil. As with other nematicides, better turf responses from Nimitz Pro G have been observed when used in conjunction with a good fungicide program. Because fluensulfone is very mobile in soil, Nimitz Pro G should not be used if heavy rain is expected in the near future, and excessive irrigation should not be applied after treatment to prevent moving the fluensulfone past the nematodes.

Conclusions

These new nematicides, along with the ones already in the arsenal, provide golf course superintendents with multiple tactics for managing nematodes. However, each new nematicide works better on some nematodes than on others. Unlike Nemacur, which worked well against all the turf nematodes, the new products require turf managers to know what kind of nematode is the primary target so that they can select the best options. Also, superintendents cannot assume that the type of nematode that was the primary problem the previous year will be the same type that is the primary problem in the current year. The nematode complex may change from year to year if only one kind of nematode is being controlled. This makes annual nematode sampling very important (3).

The potential for the development of resistance to these new nematicides is also very real. Resistance to abamectin has been well documented in mites and certain insects for decades (2), and animal-parasitic nematodes have become resistant to ivermectin (7). Various fungal species did not take long to develop resistance to the SDHI fungicide fluopyram in agriculture use (1,6). For this reason, it is highly recommended that golf courses rotate their nematicides. Fortunately, in Florida, sting, lance and root-knot nematodes can each be managed by at least two of the new nematicides, and each of these nematicides is in a different chemical class. In the case of the Pacific shoot-gall nematode, use of Indemnify should be limited to one or two applications per year. Divanem might be good as a rotation product. Alternating nematicides will prolong the usefulness of these new tools.

One area where the new nematicides are far superior to Nemacur is in regard to safety. LD₅₀ is a measurement of acute toxicity. The lower the LD₅₀, the more toxic a substance is. The oral LD₅₀ (rat) for fenamiphos (in Nemacur) is 26 milligrams/kilogram; for abamectin (in Divanem), it is 310 milligrams/kilogram; and for fluensulfone (in Nimitz) and fluopyram (in Indemnify), it is >2,000 milligrams/kilogram. These new nematicides are much safer for people, require less personal protective equipment, and have less potential impact on the environment. These differences are reflected in the signal words on the respected product labels. Signal words indicate the relative hazard level for users of a pesticide. The Nemacur label featured the signal word “Danger,” reserved for the most toxic products. Divanem has the signal word “Warning” (moderately toxic), while the signal word for both Indemnify and Nimitz is “Caution,” the lowest hazard level. We are definitely moving in the right direction.

Funding

The research discussed here was funded in part by Bayer Crop Science, Syngenta Lawn and Garden, and Control Solutions (Quali-Pro).

Literature cited

1. Amiri, A., K.A. Mulvaney, L.K. Pandit and D.R. Angelis. 2017. First report of resistance to fluxapyroxad and fluopyram in Botrytis cinerea from commercial apple orchards in Washington state. Plant Disease 101(3):508.
2. Clark, J.M., J.G. Scott, F. Campos and J.R. Bloomquist. 1995. Resistance to avermectins: Extent, mechanisms, and management implications. Annual Review of Entomology 40(1):1-30.
3. Crow, B. 2017. How do I know if I have a nematode problem? USGA Green Section Record 55(9):1-6.
4. Crow, W.T. 2005. Alternatives to fenamiphos for management of plant-parasitic nematodes on bermuda-grass. Journal of Nematology 37(4):477-482.
5. Crow, W.T. 2014. Treatment zone of abamectin in golf course greens. Journal of Nematology 46:149.
6. Fernandez-Ortuno, D., A. Perez-Garcia, M. Chamorro, E. de la Pena, A. de Vicente and J.A. Tores. 2017. Resistance to the SDHI fungicides Bascalid, fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from commercial strawberry fields in Spain. Plant Disease (in press).
7. Gasbarre, L.C., L.L. Smith, J.R. Lichtenfels and P.A. Pilitt. 2009. The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the U.S. Veterinary Parasitology 166:281-285.
8. Giblin-Davis, R.M., P. Busey and B.J. Center. 1995. Parasitism of Hoplolaimus galeatus on diploid and polyploid St. Augustinegrasses. Journal of Nematology 27(4):472-477.
9. McClure, M.A., M.E. Schmitt and M.D. McCullough. 2008. Distribution, biology, and pathology of Anguina pacificae. Journal of Nematology 40(3):226-239.
10. Perry, V.G., G.C. Smart Jr. and G.C. Horn. 1970. Nematode problems of turfgrasses in Florida and their control. Florida State Horticultural Society Proceedings 83:489-492.

William T. Crow is a professor of nematology in the Entomology and Nematology Department at the University of Florida, Gainesville; and J. Ole Becker is a Cooperative Extension specialist and nematologist in the Department of Nematology, and James H. Baird is a Cooperative Extension turfgrass specialist and horticulturist in the Department of Botany and Plant Sciences at the University of California, Riverside.