Ungulate saliva inhibits a grass–endophyte mutualism

Abstract

Fungal endophytes modify plant-herbivore interactions by producing toxic alkaloids that deter herbivory. However, studies have neglected the direct effects herbivores may have on endophytes. Antifungal properties and signalling effectors in herbivore saliva suggest that evolutionary pressures may select for animals that mitigate the effects of endophyte-produced alkaloids. Here, we tested whether saliva of moose (Alces alces) and European reindeer (Rangifer tarandus) reduced hyphal elongation and production of ergot alkaloids by the foliar endophyte Epichloë festucae associated with the globally distributed red fescue Festuca rubra. Both moose and reindeer saliva reduced the growth of isolated endophyte hyphae when compared with a treatment of distilled water. Induction of the highly toxic alkaloid ergovaline was also inhibited in plants from the core of F. rubra's distribution when treated with moose saliva following simulated grazing. In genotypes from the southern limit of the species' distribution, ergovaline was constitutively expressed, as predicted where growth is environmentally limited. Our results now present the first evidence, to our knowledge, that ungulate saliva can combat plant defences produced by a grass-endophyte mutualism.

The ecology of herbivore‐induced silicon defences in grasses

“…). Equivalent research on induced defence responses to vertebrate herbivory is relatively lacking (Walters ), although Tanentzap, Vicari & Bazely () recently provided a breakthrough by demonstrating that moose and reindeer saliva could counter alkaloid defences produced as a result of a grass–endophyte mutualism. In the case of silicon defences, there has not yet been any test of whether the application of herbivore saliva induces uptake to the same extent as actual herbivory.…”

“…In common with many types of inducible plant defences, induction of silicon is often greater in response to attack by herbivores than to artificial clipping (e.g. Massey, Ennos & Hartley 2007b;Quigley & Anderson 2014), although in contrast to other types of defence (Tanentzap, Vicari & Bazely 2014), the role of herbivore saliva in the expression of silicon is unclear. It also appears to be nonlinearly related to both the frequency and intensity of damage, requiring multiple damage events and a threshold amount of biomass to be removed (Massey, Ennos & Hartley 2007b;Reynolds et al 2012).…”

“…Components of insect saliva, plant cell wall fragments and other cues create a signalling cascade which triggers a defence response, including the production of the so-called wound hormones [jasmonic acid (JA) and salicylic acid], changes in gene expression and increases in secondary metabolites (Heil & Ton 2008;Bonaventure, VanDoorn & Baldwin 2011;Stam et al 2014). Equivalent research on induced defence responses to vertebrate herbivory is relatively lacking (Walters 2010), although Tanentzap, Vicari & Bazely (2014) recently provided a breakthrough by demonstrating that moose and reindeer saliva could counter alkaloid defences produced as a result of a grass-endophyte mutualism. In the case of silicon defences, there has not yet been any test of whether the application of herbivore saliva induces uptake to the same extent as actual herbivory.…”

Salivary cues: simulated roe deer browsing induces systemic changes in phytohormones and defence chemistry in wild‐grown maple and beech saplings

“…; Schäfer et al . , ), mammalian saliva has only been used in a very few cases (Bergman ; Rooke ; Tanentzap, Vicari & Bazely ). This is the first study to report hormonal responses together with changes in a broad range of defence metabolites after browsing of tree saplings grown under field conditions.…”

“…This response is probably due to the presence of some unknown elicitors in the saliva of mammalian herbivores. Compared to studies applying insect saliva to test plant responses (Turlings et al 1993;Halitschke et al 2001;Sch€ afer et al 2011aSch€ afer et al , 2015, mammalian saliva has only been used in a very few cases (Bergman 2002;Rooke 2003;Tanentzap, Vicari & Bazely 2014). This is the first study to report hormonal responses together with changes in a broad range of defence metabolites after browsing of tree saplings grown under field conditions.…”