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

1. 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 (for example, 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. 2. 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. 3. We found that only P addition
significantly increased native caterpillar density in the field, which
corresponded to a concomitant increase in leaf damage. Contrary 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. 4. Synthesis: Our study indicates a strong control of soil P
fertility on the tritrophic 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.