Costs and benefits of hosting Epichloë endophytes: a comparison of three haplotypes in Lolium perenne with contrasting effects on two herbivores

The symbiotic relationship between Lolium perenne and Epichloe festucae var. lolii, a fungal endophyte that lives asymptomatically in its above-ground parts, benefits both the host and fungus. In an outdoor container experiment, the effects of three distinct endophyte haplotypes (AR1, AR37 and CT) on natural infestations of a root aphid, Aploneura lentisci and a mealybug Phenococcus graminicola were compared with an endophyte-free (Nil) control. Populations of these insects were suppressed in a genetically identical set of plants treated with insecticide. Over 18 months, foliar and root growth, tiller numbers and plant mortality were compared between the different endophyte treatments and between insecticide-treated and untreated plants. Hyphal densities were recorded once during the trial. Untreated plants infected with AR37 had the lowest populations of A. lentisci and P. graminicola, and the highest root and foliar growth compared with other treatments. Growth parameters of untreated plants infected with CT often exceeded that of AR1 and Nil due to low infestations of P. graminicola and lower populations of A. lentisci. Growth of Nil, AR1 and CT plants were higher in insecticide-treated than in corresponding untreated plants but was unaffected in AR37. Untreated Nil and AR1 plants had a lower survival than AR37 and CT plants. Cumulative root outgrowth for treated AR37 plants was significantly lower than for treated AR1 on three sampling occasions. These Epichloe haplotypes are primarily mutualists, although there are circumstances when they may be disadvantageous to their host. Opposing outcomes likely originate in the ecosystems in which associations evolved.