Pine invasions linked to the invasiveness of their ectomycorrhizal fungal symbionts

Nahuel Policelli and Jennifer M. Bhatnagar, Department of Biology, Boston University, Boston, MA, Jason D. Hoeksema, Department of Biology, University of Mississippi, University, MS, Jaime Moyano, Instituto de Investigaciones en Biodiversidad y Medioambiente, Consejo Nacional de Investigaciones Científicas y Técnicas – Universidad Nacional del Comahue, Grupo de Ecología de Invasiones, San Carlos de Bariloche, Argentina, Rytas Vilgalys, Department of Biology, Duke University, Durham, NC, Sasha Vivelo, Biology, Boston University, Boston, MA

Background/Question/Methods
Symbiotic soil microbes can facilitate plant invasions. However, we still do not fully understand whether the invasion capacity of plants is associated with the invasiveness of their microbial symbionts. We compiled a global database on one of the most widespread invasive plant genera, Pinus (hereafter pines), and their major fungal symbionts ­­­—ectomycorrhizal fungi (EMF) — to address whether the frequency of reported associations with invasive EMF helps explain the invasion success of pine trees. We included data from 118 papers that reported on 695 independent pine-EMF interactions, involving 194 EMF taxa and 13 pine species in their non-native range. According to the spatial location from which the EMF were sampled, we further classified the EMF species as ‘introduced’ (found in nurseries), ‘plantation’ (found inside pine plantations), ‘early-successional invasive’ (found in the invasion front), and ‘late-successional invasive’ (found in mature invasion stands). We fit multiple linear regression models using the number of naturalization sites of the pine species —a proxy of their invasiveness— as a response variable, and the frequency of association with each EMF category, together with pine aboveground traits, as explanatory variables. We also considered edaphic and climatic variables, and phylogenetic relatedness of EMF species.
Results/Conclusions
We found that successful pine species invasions are better explained by their association with invasive EMF than by aboveground plant traits that are typically used to define invasive plant species. The association with EMF was only significant for late-successional invasive EMF, implying that a subset of all the introduced EMF species might be key to sustain the invasion of their hosts once established. The multiple regression model that best explained pine naturalizations was the one that considered both the association with late-successional invasive EMF and pine aboveground traits. We also found that invasive EMF are more frequently associated with the most invasive pine species. Our results shed light on the relative importance of microbial symbionts in the invasion biology of plants, which is critical for understanding the magnitude and severity of invasions and for mitigating their impacts and restoring native habitats.