Novel interactions between non‐native mammals and fungi facilitate establishment of invasive pines

Abstract

Summary1. The role of novel ecological interactions between mammals, fungi and plants in invaded ecosystems remains unresolved, but may play a key role in the widespread successful invasion of pines and their ectomycorrhizal fungal associates, even where mammal faunas originate from different continents to trees and fungi as in New Zealand. 2. We examine the role of novel mammal associations in dispersal of ectomycorrhizal fungal inoculum of North American pines (Pinus contorta, Pseudotsuga menziesii), and native beech trees (Lophozonia menziesii) using faecal analyses, video monitoring and a bioassay experiment. 3. Both European red deer (Cervus elaphus) and Australian brushtail possum (Trichosurus vulpecula) pellets contained spores and DNA from a range of native and non-native ectomycorrhizal fungi. 4. Faecal pellets from both animals resulted in ectomycorrhizal infection of pine seedlings with fungal genera Rhizopogon and Suillus, but not with native fungi or the invasive fungus Amanita muscaria, despite video and DNA evidence of consumption of these fungi. 5. Native L. menziesii seedlings never developed any ectomycorrhizal infection from faecal pellet inoculation. 6. Synthesis. Our results show that introduced mammals from Australia and Europe facilitate the co-invasion of invasive North American trees and Northern Hemisphere fungi in New Zealand, while we find no evidence that introduced mammals benefit native trees or fungi. This novel tripartite 'invasional meltdown', comprising taxa from three kingdoms and three continents, highlights unforeseen consequences of global biotic homogenization.

Suilloid fungi as global drivers of pine invasions

“…There is also experimental evidence of a similar three‐way interaction in New Zealand, where non‐native Australian possums disperse non‐native European and North American suilloid fungi (species of Rhizopogon and Suillus ), facilitating North American pine establishment (Wood et al ., ). Native EMF can also be consumed by non‐native invasive mammals, but current evidence shows that they are not capable of readily colonizing either native or invasive tree species (Wood et al ., ). Interestingly, studies from South America show that native mammals (rodents and a native dwarf deer Pudu pudu ) do not play a significant role in dispersing non‐native fungi because of the scarce abundance of these animals (Nuñez et al ., ).…”

Mycorrhizal co‐invasion and novel interactions depend on neighborhood context

“…Successful establishment and invasion of woody plants may be particularly sensitive to belowground symbiont availability, because many of these woody plant species depend on mutualistic microbes like mycorrhizal fungi and nitrogen-fixing bacteria (Nun˜ez and Dickie 2014). In fact, recent research has revealed that both co-invasion of nonnative mutualist species and novel associations with native species determine invasion success (Pringle et al 2009, Dickie et al 2010, Nun˜ez and Dickie 2014, Wood et al 2015. For example, ectomycorrhizal pines appear to invade only when co-invading exotic or cosmopolitan fungi are available (Nun˜ez et al 2009, Dickie et al 2010, Hynson et al 2013, Hayward et al 2015, though introduced trees may form novel associations with native fungi as adults (Parlade´et al 1995, Jairus et al 2011, Trocha et al 2012, Bahram et al 2013.…”

Impacts of invasive biota in forest ecosystems in an aboveground–belowground context

“…For example, invasive woody plants may be dependent on co-invasion by invasion of their mutualists such as nitrogen fixing bacteria or ectomycorrhizal fungi (Nuñez and Dickie 2014;Traveset and Richardson 2014). Recent studies have also shown that invasive mammals can in turn facilitate the dispersal of invasive ectomycorrhizal fungal species required for the successful establishment of invasive tree species, in both Argentina (Nuñez et al 2013) and New Zealand (Wood et al 2015). Such studies provide evidence the effect of invasive organisms on ecosystem properties can be dependent on, or exacerbated by, co-invasion by other organisms, although this has been explicitly addressed in few studies.…”