Do fungicide applications have bottom-up effects on soil arthropods?

Golf courses are intensively managed and require constant input of fungicide to control fungal pathogens. However, little is known of the long-term effects of fungicide application on the community structure and function of beneficial soil organisms. In this study, we investigate the consequence of fungicide application history on root-symbiotic and saprotrophic fungal communities, and whether such effects could cascade up to influence the density and composition of fungal-feeding arthropods in soils. We also explore whether changes in the community of these soil organisms would have further effects on ecosystem processes. We hypothesized that mycorrhizal and endophytic fungal abundance will be reduced under high fungicide application rates, and predicted that the reduction in fungal abundance would further suppress soil arthropods that rely on fungal hyphae and spores as food resources.

Eight golf courses were selected in Central NY State, and divided into three groups based on the levels of past and current fungicide application: none, low and high fungicide intensity. In May and September 2014, three fairways were randomly selected from each golf course, and 5 pairs of soil cores (5 cm in diameter x 5 cm deep) were collected from each fairway. In addition, samples were also collected from three undisturbed meadows in the same region for comparison of soil organisms from natural habitats. Half of the soil cores were placed in Berlese funnels to extract arthropods. The other 5 cores were kept for further analyses of fungal infections in roots and enzyme activities in rhizosphere soils.

Overall, the abundance of root-infecting fungi varied among sampling seasons and fungicide application intensities. Fungicide application suppressed AMF infection in spring by 25% in percentage of roots colonized (an average of 44% in high fungicide treatment vs. 19% in zero fungicide treatment, P = 0. 015). While fungicide application did not seem to affect AMF infection in September, there was a trend of increasing total fungal infection (including AMF and endophytic fungi) with reducing fungicide input. In addition, activities of five common enzymes (chitinase, cellulase, peptidase, phosphatase, and phenol oxidase) showed distinct differences between golf courses with high fungicide and zero fungicide treatments (golf courses and meadows); and this separation was mainly driven by the lower phosphatase activity under high fungicide application. Abundance of soil arthropods was generally high in golf courses (ranging from 10,000 to over 40,000 individuals m^-2); however, fungicide application rate appeared to have little effect on the density of major fungivorous taxa including Collembola and oribatid mites (P > 0.1). Our results suggest that long-term application of fungicide in golf courses suppresses root-associated fungi with potential consequence in soil nutrient cycling by affecting enzyme activities.