Discovering the Role of Patagonian Birds in the Dispersal of Truffles and Other Mycorrhizal Fungi

Abstract

Dispersal is a key process that impacts population dynamics and structures biotic communities. Dispersal limitation influences the assembly of plant and microbial communities, including mycorrhizal fungi and their plant hosts. Mycorrhizal fungi play key ecological roles in forests by feeding nutrients to plants in exchange for sugars, so the dispersal of mycorrhizal fungi spores actively shapes plant communities. Although many fungi rely on wind for spore dispersal, long-distance dispersal is uncommon and most spores land close to fungal fruiting bodies. Some fungi have lost the ability to shoot their spores into the air and instead produce enclosed belowground fruiting bodies (truffles) that rely on animals for dispersal. Animal-facilitated spore dispersal increases the chances that spores reach suitable habitats and colonize plant roots. The role of mammals in fungal spore dispersal is well documented but the relevance of birds as dispersal agents of fungal spores has been understudied, despite the prominence of birds as seed dispersal vectors. Here we use metagenomics and epifluorescence microscopy to demonstrate that two common, widespread and endemic birds from Patagonia, Chucao Tapaculos (Scelorchilus rubecula) and Black-throated Huet-huets (Pteroptochos tarnii), regularly consume mycorrhizal fungi and disperse viable spores via mycophagy. We sampled more than 100 fecal samples that were collected across a 700 kilometer area in Patagonia. Our metagenomic analysis indicates that these two species of generalist, ground-dwelling birds routinely consume diverse mycorrhizal fungi, including many truffles, that are symbiotically associated with Nothofagaceae trees that dominate Patagonian forests. We used soil sample controls to ensure that fecal samples were not contaminated from nearby soil as well as extraction, PCR and sequencing controls to account for lab contamination. Epifluorescence microscopy of fecal samples confirmed that the birds dispersed large numbers of viable spores from truffles and other mycorrhizal fungi, including Cystangium nothofagi and species of Cortinarius, Descolea, and Inocybe, which are important root colonizers of seedling and saplings of several Nothofagaceae species. Our results show that fungi are a common food for both bird species and that this cryptic animal-fungi symbiosis is widespread and ecologically important in Patagonia. Our findings suggest that birds may also act as cryptic but critical agents of fungal spore dispersal in other ecosystems.