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

Abstract

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 (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. 2. We explored the relative and interactive importance of soil nitrogen (N) and phosphorus (P) in modulating the interaction of the invasive grass tall fescueassociated 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 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. 4. 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 endophytesymbiotic forage plants in natural grasslands.

Landscape variation in defense traits along gradients of multiple resources in a tropical savanna plant

“…Our results on the positive association between soil P and prickle density (Fig. 2c) adds to the evidence from earlier research on insect herbivores showing that P supply may affect anti‐herbivore defenses (Cuevas‐Reyes et al 2004, 2011, De Long et al 2016, Graff et al 2020). However, the proximate mechanisms still remain unclear.…”

Soil fertility as a mediator of interactions between an introduced specialist beetle and a native generalist nematode on an exotic invasive plant and its native congener

“…Soil fertility can mediate the performance of herbivores on both native and invasive plants (Sun et al., 2010) because the levels of nutrients in the soil may strongly affect the resistance or susceptibility of plants to herbivores (Gao et al., 2021; Liang et al., 2020; Yuan et al., 2013). Soil fertility can also potentially alter the interactions of herbivores with invasive plants either directly or indirectly by altering herbivore abundance (Graff et al., 2020), degree of damage to the plant (Lu et al., 2015), species distributions (Vavra et al., 2007) and synchrony with hosts (Hultine et al., 2015). Furthermore, the effects of soil N and P availability and the levels of herbivore damage can interactively determine the success of an invasion and the following ecological interactions in the introduced range (Driscoll & Strong, 2018; Graff et al., 2020).…”

Restoration of invaded temperate grasslands: species phenology adds to microsite and seed availability

“…Here, grazing exclusion was traditionally used to recover native communities (Chaneton & Facelli, 1991). However, recent evidence stresses the increasing invasion of Festuca arundinacea (hereafter, tall fescue) in grazing exclosures (Graff et al, 2020), which may preclude the passive establishment of native functional groups. The maximum rate of growth of the tall fescue occurs in spring when its leaves are growing the most and culminates in flowering (Scheneiter & Améndola, 2012).…”