Microbial stowaways: Waterbirds as dispersal vectors of aquatic pro‐ and microeukaryotic communities

Abstract

Aim Waterbirds are important dispersal vectors of multicellular organisms; however, no study to date has focused on their potential role in dispersing aquatic microbial communities. We explicitly studied endozoochory of prokaryotes and unicellular microeukaryotes by waterbirds using DNA metabarcoding. By directly comparing the dispersed set of organisms to the source pool of a natural metacommunity, we aimed at a realistic estimate of the importance of waterbird zoochory for natural microbial communities. Location Temporary saline soda pans in Austria and Hungary. Taxon Prokaryotes and unicellular microeukaryotes. Methods In 2017 and 2018, water samples were collected from a network of 25 temporary ponds along with fresh droppings of five waterbird species including the dominant greylag goose (Anser anser). Prokaryotic and microeukaryotic communities were identified via 16S and 18S rRNA gene amplicon sequencing. After quality filtering of sequence reads, pro‐ and microeukaryotic amplicon sequence variant (ASV) compositions were compared between the aquatic and dropping samples, across years and waterbird species. Results 28% of the dominant aquatic prokaryotic and 19% of the microeukaryotic ASVs were transported by A. anser. ASV richness was lower, but compositional variation was higher in A. anser droppings than in aquatic communities, probably resulting from stochastic pick‐up from multiple aquatic habitats. The composition of prokaryotic ASVs in bird droppings differed among the 2 years and reflected the actual aquatic communities. The dispersed set of microbes were largely similar among the waterbird species except for the planktivore filter‐feeder northern shoveler (Spatula clypeata), which dispersed more microeukaryotes than the other waterbirds. Main conclusions Using an amplicon sequencing approach to characterize aquatic microorganisms in waterbird droppings and in the associated environment, our study provides strong evidence for endozoochory of natural communities. These results imply that waterbirds may be crucial in maintaining ecological connectivity between aquatic habitats at the level of microbial communities.

Dispersal of aquatic and terrestrial organisms by waterbirds: A review of current knowledge and future priorities

“…In the future, there needs to be far more research into microbial dispersal by waterbirds. In particular, there is a need to further clarify which of the microbes detected in barcoding studies of faeces or feathers are viable, and what influence the microbes carried by birds have on pre‐established microbial communities, compared to inputs from air or water (Custer et al, 2022; Szabó et al, 2022). The meta‐gut concept should be explored, comparing gut microbiomes of waterbirds and co‐existing aquatic organisms (Dutton et al, 2021).…”

“…Like the nostrils of seabirds (Brito-Echeverria et al, 2009), the feathers of flamingos are rich in haloarchaea, which presumably disperse with flamingos when they undergo long-distance movements (Yim et al, 2015). There is evidence for major exchange between the microbial communities carried in waterbird guts and those present in the lakes they visit (Szabó et al, 2022), suggesting that waterbirds may be vital in maintaining connectivity in microbial lake metacommunities, and that their gut microbiomes might influence lake biogeochemistry, as well as the gut microbiomes of other aquatic organisms (the "meta-gut" concept; Dutton et al, 2021).…”

Environmental changes associated with drying climate are expected to affect functional groups of pro- and microeukaryotes differently in temporary saline waters

“…Our results demonstrated that soda pans host diverse microbial communities, which were so far largely unexplored due to the lack of regional studies and the limited application of molecular methods. Even though these unique and regionally restricted ecosystems serve as important refuges for a number of rare or endangered species (Horváth et al ., 2013; Stenger-Kovács and Lengyel, 2015), and serve as important feeding sites for waterbirds (Boros et al ., 2017; Szabó et al ., 2022), they are critically endangered by climate change (Horváth et al ., 2019). The ongoing environmental changes will most likely lead to biodiversity loss in multiple microbial groups according to our results, which might induce critical ecosystem-level consequences.…”

“…For the determination of prokaryotic and eukaryotic community composition, the V4 region of the 16S rRNA gene and the V7 region of the 18S rRNA gene were amplified, using prokaryotic primers EMBf 515F (GTGYCAGCMGCCGCGGTAA, Parada, Needham and Fuhrman, 2016) – EMBr 806R (GGACTACNVGGGTWTCTAAT, Apprill et al ., 2015) and eukaryotic primers UnivF-1183mod (AATTTGACTCAACRCGGG) – UnivR-1443mod (GRGCATCACAGACCTG, Ray et al ., 2016). All polymerase chain reactions and amplicon sequencing (Illumina MiSeq platform) were carried out by LGC Genomics (Berlin, Germany) following the steps described in Szabó et al ., 2022 (Table S3).…”

Ciliates in man-made mountain reservoirs

“…However, it is unknown how urotrichs are dispersed among water bodies as cyst formation has so far never been observed. We therefore exclude wind drift, but a direct transport in water drops or faeces via birds (Szabó et al, 2022) may be possible as birds were occasionally seen at the mountain reservoirs. Alternatively, urotrichs could be washed out from the vegetation cover in the surroundings of the mountain reservoirs as, for example, in seepage and fen areas of the Rotmoos valley near the SWH, urotrichs were frequently observed (Sonntag, unpublished).…”