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Key Takeaways

  • Results from this study verify reports from superintendents that fluopyram resistance is occurring among multiple nematode species on golf courses in Florida.

  • Fluopyram did not work nearly as well on sting and root-knot nematodes collected from golf courses with a history of extensive, repeated use of SDHI nematicides compared to sites that have never used it.

  • Nematicides should be rotated among chemical classes each year to avoid the onset of resistance, so golf courses can continue taking advantage of the most effective nematicide options.


     

Indemnify (fluopyram) was launched in the U.S. turf market in 2016 and quickly became the nematicide of choice for many golf course superintendents struggling against plant-parasitic nematodes. Fluopyram is a succinate dehydrogenase inhibitor (SDHI) nematicide and is also an active ingredient in Envu’s turfgrass fungicides Resilia and Exteris Stressgard. Research has shown fluopyram to be highly effective against most plant-parasitic nematodes that damage golf turf including root-knot, sting and shoot-gall nematodes (Crow et al., 2017). However, by 2019 some golf course superintendents in Florida began reporting that it was not working as well as it had at first. To investigate this, the USGA funded research at the University of Florida to determine if reduced efficacy from fluopyram was a real phenomenon, and if so, what was the likely mechanism.

Nematicide Use, Degradation and Resistance

Until 2019, there had never been a reported incidence of nematicide resistance in plant-parasitic nematodes, but enhanced degradation of certain older nematicides like fenamiphos (Nemacur) was a common issue. Resistance means that a large percentage of the target pest population does not respond to the pesticide, whereas enhanced degradation means that microbes in the soil break down the pesticide so rapidly that it doesn’t work like it should.

The Insecticide Resistance Action Committee (IRAC) Nematode Working Group released a nematicide resistance risk statement listing several reasons why plant-parasitic nematodes have low risk to develop nematicide resistance. However, many of the reasons listed – e.g., seed treatments, crop rotation and use of resistant plant varieties – are not applicable to how SDHI nematicides are used on turf (IRAC Team, 2021). In addition, agricultural nematicides are typically applied only once per growing season while in golf settings they can be applied up to four times per year. Finally, unlike agricultural crops, golf turf consists of a continuous stand of uniform grass and SDHI nematicides (IRAC Group N-3) are very long-lived, with a half-life of over a year and bioavailability of six months or more. This means multiple nematode generations over a long period are potentially exposed, increasing the chance of resistance even more. Therefore, the reasons that plant-parasitic nematodes are considered as low risk for nematicide resistance in agricultural settings are not relevant to golf turf. To get to the bottom of the reduced effectiveness of fluopyram reported by superintendents, the University of Florida initiated experiments to investigate.
 

Investigating Fluopyram Resistance

To conduct the research, soil and nematodes were collected from multiple sources. One source was a replicated field trial at the University of Florida Plant Science Unit in Citra, Florida, that had plots where Indemnify had never been used, plots where Indemnify at the spot-treatment rate (0.39 fluid ounces of product per 1,000 square feet) had been applied four times per year for four years, and plots where Indemnify had been applied four times in one year. A second source of nematodes and soil was from commercial turfgrass locations in Florida where Indemnify and fluopyram-containing fungicides had either never been used or where Indemnify had been used regularly for several years.

Could Degradation Be the Cause?
The first round of experiments evaluated the soil from these different locations looking for evidence of enhanced degradation. With repeated use of a certain product, microbe populations in the soil will shift to those that preferentially feed on it, resulting in enhanced degradation. These experiments revealed that fluopyram applied to soil from research plots and golf greens where Indemnify had often been used persisted equally well as in soils with no previous fluopyram exposure (Kammerer et al., 2023). Therefore, we concluded there was no evidence of enhanced degradation.

SDHI Resistance Studies
The second round of experiments looked for evidence of resistance. Grass root-knot nematode (Meloidogyne graminis) populations were collected from the research plots and from the commercial turf sites and brought to the lab. The nematodes were placed in small observation wells and exposed to 8 or 16 ppm of fluopyram for 24 and 72 hours. After that, a stimulant was added to make any live nematodes start moving. Any nematodes that remained straight and motionless were considered dead, and the percent mortality was determined by dividing the number of immobile nematodes by the total number of nematodes in the well. This experiment revealed that the nematodes from research plots or golf greens where Indemnify was used previously were less responsive to fluopyram than the nematodes from research plots and golf courses where Indemnify had not been used previously (Figure 1). These results indicate that fluopyram resistance is occurring.
 

Next, two populations of grass root-knot nematode and three populations of sting nematode (Belonolaimus longicaudatus) were collected from several of the golf courses where Indemnify had been used repeatedly and from golf courses where Indemnify had not been used. These nematode populations were inoculated onto bermudagrass and maintained in a greenhouse on the University of Florida campus. There were two populations of previously exposed root-knot nematodes and two populations that had not been exposed to fluopyram, and three previously exposed populations of sting nematode and three non-exposed populations. These nematodes were then extracted and exposed to 10 or 50 ppm fluopyram in microwells for 24 or 72 hours and percent mortality was determined as described for the preceding experiment. In this experiment, the percent mortality of both root-knot and sting nematode populations originating from locations with a history of fluopyram use was greatly reduced compared to nematodes from sites that had never used fluopyram (Figure 2).

These results verify that fluopyram resistance is occurring in multiple nematode species on golf courses in Florida following extensive fluopyram use. Recently, scientists with Bayer Crop Science also reported fluopyram resistance in root-knot nematodes in agriculture in Europe.

While this research has focused on fluopyram since it is the first SDHI nematicide on the market, resistance concerns go beyond this one active ingredient. Resistance will likely be an issue for other SDHI nematicides as they become available too. Also, cross-resistance is a possibility, so if nematodes develop resistance to one nematicide they may also be resistant to other nematicides in the same class.

Implications for Golf Courses

What do these results mean to golf course superintendents? It is critical that nematicide applications be rotated among chemical classes to avoid resistance and prolong the usefulness of the most effective nematicide options. A multiyear research project is underway at the University of Florida to evaluate nematicide programs for resistance management and efficacy against sting and root-knot nematodes – the most important nematodes on warm-season turfgrass. Currently, University of Florida recommendations are to not use SDHI nematicides two years in a row, but to use nematicides from other classes every other year (Crow, 2024). Some effective rotation partners that are currently available for managing sting and root-knot nematodes on warm-season turf are shown in the table below. Additional effective nematicides from different classes should be coming in the near future.
 

Nematicides have come a long way, and the new generation of products offer more variety and are safer to use than the old organophosphate nematicides like fenamiphos (Nemacur). A second SDHI nematicide, cyclobutrifluram from Syngenta Crop Protection, is scheduled for launch in the U.S. soon and other companies also have SDHI nematicides in development. They are very effective for managing most problematic nematodes on golf courses and their use will be foundational for nematode management programs going forward. However, just because SDHI nematicides can be considered among the most effective does not mean they should be used all the time. They should be used sparingly and rotated with nematicides from other classes to preserve their effectiveness.

References

Crow, W. T., Becker, J. O., & Baird, J. H. (2017). New golf course nematicides. Golf Course Management, 85, 66-71.

Crow, W. T. (2024). Nematode management for golf courses in Florida. UF/IFAS Electronic Data Information Source. https://edis.ifas.ufl.edu/publication/IN124

IRAC Nematodes Team (2021). Nematicide resistance risk statement. Insecticide Resistance Action Committee. https://irac-online.org/documents/nematicide-resistance-risk-statement/?ext=pdf

Kammerer, C. L., Harmon, P. F., & Crow, W. T. (2023). Reduced sensitivity to fluopyram in Meloidogyne graminis following long-term exposure in golf turf. Journal of Nematology, 55: e2023-0048.