Protection offered by leaf fungal endophytes to an invasive species against native herbivores depends on soil nutrients

Abstract

Natural grassland ecosystems are increasingly threatened by excessive loadings of nutrients and by the presence of species bred for high productivity. By manipulating grazing regimes and nutrient availability, agricultural practices facilitate the establishment and spread of certain forage plant species outside managed landscapes, challenging local biodiversity. The ecological success of some species in the invaded range sometimes seems to be associated with the symbiosis with foliar fungal endophytes. Symbiotic fungi may increase the competitiveness of host species, but also the resistance to herbivory through the production of toxic secondary compounds such as alkaloids. While progress has been made in understanding how soil nutrients modulate other benefits offered by fungal endophytes to plants (e.g. stress tolerance, competitive ability, etc), the consequences for a higher trophic level (i.e. herbivores) and the potential feedbacks on plant invasion have not been explored yet. We explored the relative and interactive importance of soil nitrogen (N) and phosphorus (P) in modulating the interaction of the invasive grass tall fescue—associated with fungal endophytes—and native herbivores in a natural grassland. We hypothesized that N and P nutrients modulate differentially leaf quality traits, namely nutritional value and fungal alkaloid contents, determining the level of damage by native insect herbivores on the exotic tall fescue. We found that only the addition of P significantly increased native caterpillar density in the field, which corresponded to a concomitant increase in leaf damage. In contrast to expectations, the concentration of the alkaloid ergovaline in leaves was not strongly related to N. It was the level of soil P which dictated the concentration of the element (P) in the leaves and reduced the level of defence against herbivores in this endophyte-symbiotic species. Then, herbivore performance increased, and plants were more prone to be attacked. Synthesis. Our study indicates a strong control of soil P fertility on the triple interaction among plants, fungal endophytes and native herbivores. This highlights the potential role of increased soil nutrients on the invasion spread of endophyte-symbiotic forage plants in natural grasslands.