Microbial stowaways – waterbirds as dispersal vectors of aquatic pro- and microeukaryotic communities

Abstract

Aim: Waterbirds are important dispersal vectors of multicellular organisms such as macrophytes, aquatic macroinvertebrates, and zooplankton. However, no study to date has focused on their potential role in dispersing aquatic microbial communities. Here, we carried out the first explicit study on passive transport (endozoochory) of prokaryotes and unicellular microeukaryotes by waterbirds based on a metagenomic approach. By directly comparing the dispersed set of organisms to the source pool of a natural metacommunity, we aimed for a realistic estimate of the overall importance of waterbird zoochory for natural microbial communities. Location: Seewinkel region of Austria and Hungary. Taxon: Prokaryotes and unicellular microeukaryotes. Methods: In 2017 and 2018, water samples from natural aquatic habitats along with fresh droppings of the dominant greylag goose (Anser anser) and four other waterbird species were collected in a well-delineated habitat network of temporary saline ponds (soda pans). Their prokaryotic and microeukaryotic communities were identified via 16S and 18S rRNA gene amplicon sequencing and compared across years and waterbird species. Results: We found that up to 40% of the dominant aquatic microbial OTUs were transported by A. anser. OTU richness in A. anser droppings was lower, but compositional variation was higher compared to the aquatic communities, probably resulting from stochastic pick-up of microbes from multiple aquatic habitats. We furthermore found that prokaryote species composition of bird droppings followed the interannual turnover in the aquatic communities. Finally, we found species-specific differences among different waterbird species. Among them, the planktivore filter-feeder northern shovelers (Anas clypeata) collected and dispersed a more species-rich subset of microeukaryotes than shorebirds or geese. Main conclusions: Overall, our study provides the first quantitative empirical evidence of endozoochory in natural microorganism communities. These results imply that waterbirds may be crucial in maintaining ecological connectivity between discrete aquatic habitats at the level of microbial communities. Keywords: aquatic microorganisms, bacteria, connectivity, dispersal, endozoochory, phytoplankton, protists, waterbirds