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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. [ABSTRACT FROM AUTHOR]

1. The strength of many interactions between plants and other organisms changes across regional gradients. For example, the relevance of plant-herbivore interactions increases with primary production. Likewise, biotic interactions collectively become more intense from the poles to the equator. Yet, the regional variation of the interaction between grasses and systemic fungal endophytes, which provide resistance to biotic and abiotic environmental factors (i.e. herbivory and drought), is poorly understood. 2. We compiled 1008 records of the incidence level of fungal endophytes (Epichloë, Ascomycetes: Clavicipitaceae) on wild populations of 48 cool season grasses, encompassing 10 biomes across a broad latitudinal expanse and primary production gradient. Symbiosis incidence was analysed as a function of mean primary production, precipitation, temperature and latitude of each site, which in turn were obtained from climatic and satellital sources. 3. Across a 30-fold variation of mean primary production, average symbiosis incidence increased from 20% to 70%. The pattern became stronger when the analysis was restricted to the single grass genus Festuca, which accounted for half of the total data. 4. The number of grass populations showing no symbiosis incidence (0%) decreased as primary production increased, whereas those with 100% of incidence increased. 5. Primary production at the regional scale was negatively correlated with latitude but positively with mean annual temperature and precipitation. Symbiosis incidence was similarly correlated with latitude and temperature, and it was not with mean annual precipitation. 6. Synthesis. Different descriptors of this grass-fungus symbiosis show that average incidence in wild populations world-wide increases with mean primary production. As at large spatial scales herbivory and temperature increase and aridity decreases with primary production, our results suggest that, at broad-scales, these biotic and abiotic factors may be important drivers of the symbiosis success. [ABSTRACT FROM AUTHOR]

The most studied mechanism of protection against herbivores in grasses associated with Epichloë fungal endophytes has been the fungal production of alkaloids. However, the contribution of the plant immune response on the level of resistance to herbivores in symbiotic grasses has been poorly explored. We studied the relationship between the plant hormone, jasmonic acid (JA) and Epichloë fungal endophytes on herbivore defences in symbiotic grasses. We hypothesized that an exogenous application of methyl jasmonate (MeJA), an activator of the plant JA defence response, would increase the level of resistance of endophyte‐symbiotic and non‐symbiotic plants to a chewing insect. As Epichloë endophytes produce alkaloids, an enhancement of the JA defence would complement the resistance given by these alkaloids.Lolium multiflorum plants symbiotic and non‐symbiotic with the endophyte Epichloë occultans were subjected to an exogenous application of MeJA followed by a challenge with the generalist chewing insect Spodoptera frugiperda. We measured the level of plant resistance to chewing insects, and the defences conferred by host plants and fungal endophytes.Symbiotic plants were more resistant to S. frugiperda than their non‐symbiotic counterparts. However, despite the fact that the concentration of JA significantly increased in all plants exposure to MeJA, neither endophyte‐symbiotic nor non‐symbiotic plants showed an enhanced resistance to insects. Unexpectedly, the exposure of endophyte‐symbiotic plants to MeJA led to a reduction in the concentration of loline alkaloids (i.e. N‐formyllolines and N‐acetylnorlolines), consequently decreasing the level of plant resistance to the herbivore.Synthesis. Our results suggest that, rather than complementing the alkaloid‐based defence, the jasmonic acid hormone weakens the anti‐herbivore mechanism conferred by Epichloë endophytes. The present study highlights that the interaction between the jasmonic acid hormone and the presence of leaf fungal endophytes can be of importance for the effectiveness of the anti‐herbivore defences of symbiotic plants. Our results suggest that, rather than complementing the alkaloid‐based defence, the jasmonic acid hormone weakens the anti‐herbivore mechanism conferred by Epichloë endophytes. The present study highlights that the interaction between the jasmonic acid hormone and the presence of leaf fungal endophytes can be of importance for the effectiveness of the anti‐herbivore defences of symbiotic plants. [ABSTRACT FROM AUTHOR]