Alkaloids may not be responsible for endophyte‐associated reductions in tall fescue decomposition rates

Abstract

Summary1. Fungal endophyte -grass symbioses can have dramatic ecological effects, altering individual plant physiology, plant and animal community structure and function, and ecosystem processes such as litter decomposition and nutrient cycling. 2. Within the tall fescue (Schedonorus arundinaceus) -fungal endophyte (Neotyphodium coenophialum) symbiosis, fungal produced alkaloids are often invoked as the putative mechanism driving these ecological responses. Yet few measurements of alkaloids exist in the ecological literature. In this study, we quantified alkaloid levels in live, standing dead and decomposing endophyte-infected (E+) and -free (E)) plant material and simultaneously evaluated the direct and indirect effects of endophyte presence on tall fescue decomposition. 3. Loline and ergot alkaloid levels were consistently high in live E+ (common toxic strain of N. coenophialum) tall fescue biomass throughout the sampling period (May-November 2007), whereas, E) live and standing dead material had non-detectable alkaloid concentrations. Standing dead E+ biomass had significantly reduced alkaloid levels (6-19x lower than the levels measured in the corresponding live E+ biomass) that were equivalent to E) live and dead for loline but were still somewhat higher than E) material for ergots. 4. In an effort to test the role of alkaloids in directly inhibiting decomposition, as has been suggested by previous studies, we conducted a litter bag experiment using green, alkaloid-laden E+ and alkaloid-free E) tall fescue plant material. We incubated E+ and E) litter bags in both E+ and E) tall fescue stands for 170 days, and measured mass loss, carbon and nitrogen content, and ergot and loline alkaloid concentrations over the incubation period. 5. Consistent with previous reports, both direct and indirect effects of endophyte presence on litter decomposition were observed: endophyte presence in the litter and surrounding microenvironment significantly reduced decomposition rates. Surprisingly, despite large differences in alkaloid content between E+ and E) litter from Day 0-Day 21 of the incubation, direct effects of the endophyte on litter decomposition, while significant, were relatively small (differences in mass loss between E+ and E) litter were never >3%). Alkaloids were gone from E+ material by day 56. 6. We propose that results from this study indicating alkaloids are largely absent in standing dead material (the typical input to the decomposition process), and that despite being present in our litter bag experiment, failed to produce large differences in mass loss between E+ and E) material questions the supposition that fungal produced alkaloids directly inhibit decomposition. Additional studies exploring the mechanisms behind the direct and indirect effects of endophytes on this ecosystem process are needed.

No effects of Epichloë endophyte infection on nitrogen cycling in meadow fescue (Schedonorus pratensis) grassland

“…This shows that litter N%, even when originating from the limited spatial variation of a homogeneous agricultural soil, can be a main control of litter decomposition and N cycling in grasslands. Since litter N% was not affected by grass endophyte infection in our study, litter N% could not mask any potential alkaloid effects, but such mask is possible in other studies as the endophyte infection has been shown to increase grass green leaf N% (Siegrist et al 2010;Vázquez-de-Aldana et al 2013). In fact, Siegrist et al (2010) speculated that the weak effect of high alkaloid concentrations on decomposition in their study with green leaf material was due to the high N% of the material, which potentially alleviated the adverse alkaloid effects.…”

“…There is also evidence of lower microbial activity and accumulation of organic matter under endophyte infected grass (Franzluebbers et al 1999). These effects are assumed to be due to the alkaloids having adverse effects on soil decomposers (Franzluebbers et al 1999), but this assumption has also been questioned in a study, where high alkaloid concentrations of green grass leaves had only a small negative effect on leaf decomposition in comparison to green leaves with no alkaloids (Siegrist et al 2010). Further investigations of the effects of Epichloë infection on grass litter decomposition are therefore needed (Omacini et al 2012), and so far no study has tested whether the Epichloë effects on litter mass loss translate to changes in nutrient cycling in plant communities with Epichloë infected grasses.…”

“…The systemic Epichloë endophytes (including the fungi earlier classified in Neotyphodium; Leuchtmann et al 2014), which are common among the cool season Poaceae grasses (subfamily Pooideae) (Schardl et al 2011), are particularly well known for their abundant production of alkaloids (Lehtonen et al 2005;Saikkonen et al 2013a) that protect their grass hosts against pathogens and herbivores (Clay 1988;Clay and Schardl 2002). Like the secondary metabolites of plant leaves, these alkaloids remain in senescent grass leaves (Siegrist et al 2010) and are therefore assumed to have effects on litter decomposition and nutrient cycling (Saikkonen et al 2015). There are few studies that have examined the effects of Epichloë infection on grass litter decomposition, but so far all published studies have found a weak, negative effect on litter mass loss (Omacini et al 2004;Lemons et al 2005;Siegrist et al 2010).…”

“…Based on the earlier findings of reduced litter mass loss in Epichloë infected Italian ryegrass, Lolium multiflorum (Omacini et al 2004) and tall fescue, Schedonorus arundinaceus (syn. Festuca arundinacea and Lolium arundinaceum) (Lemons et al 2005;Siegrist et al 2010), we hypothesized that (1) E. uncinata infection will decelerate the decomposition rate of meadow fescue shoot litter, and as a result, (2) more organic C and N will accumulate in the soil in E+ than E-plots (Franzluebbers et al 1999), (3) less N will be released from E+ than E-litter and (4) less mineralized N (NH 4 and NO 3 ) will be available in the soil under E+ than E-plants. However, since microbial communities can express home field advantage (Austin et al 2014), we also predicted that the mass loss and N release of E+ litter would be higher in the E+ than E-plots.…”

“…Like the secondary metabolites of plant leaves, these alkaloids remain in senescent grass leaves (Siegrist et al 2010) and are therefore assumed to have effects on litter decomposition and nutrient cycling (Saikkonen et al 2015). There are few studies that have examined the effects of Epichloë infection on grass litter decomposition, but so far all published studies have found a weak, negative effect on litter mass loss (Omacini et al 2004;Lemons et al 2005;Siegrist et al 2010). There is also evidence of lower microbial activity and accumulation of organic matter under endophyte infected grass (Franzluebbers et al 1999).…”