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Biodiversity loss threatens ecosystems and human well-being, making accurate, large-scale monitoring crucial. Environmental DNA (eDNA) has enabled species detection from substrates such as water, without the need for direct observation. Lately, airborne eDNA has been showing promise for tracking organisms from insects to mammals in terrestrial ecosystems. Conventional biodiversity assessments are often labor-intensive and limited in scope, leaving gaps in our understanding of ecosystem response to environmental change. Here, we demonstrate that airborne eDNA can detect organisms across the tree of life, quantify changes in abundance congruent with traditional monitoring, and reveal land-use induced regional decline of diversity in a northern boreal ecosystem over more than three decades. By analyzing 34 years of archived aerosol filters, we reconstruct weekly temporal relative abundance data for more than 2700 genera using non-targeted methods. This study provides unified, ecosystem-scale biodiversity surveillance spanning multiple decades, with data collected at weekly intervals on both the individual species and community level. Previously, large scale analyses of ecosystem changes, targeting all types of organisms, has been prohibitively expensive and difficult to attempt. Here, we present a way of holistically doing this type of analysis in a single framework.

Bryophytes constitute a diverse plant group with important roles in ecosystem functioning, in particular in arctic and subarctic environments. As they are physiologically strongly dependent on climatic conditions bryophytes could serve as indicators of ongoing climatic change. Their spores are generally dispersed by wind, and because of contrasting phenologies among species, the composition of the spore cloud changes throughout the year. Unlike vascular plant pollen, airborne bryophyte spores have few specific morphological characteristics, and therefore spore dispersal phenology has, until now, relied on highly laborious in situ observations.

Here, we report on multi-decadal shifts in the phenology of spore dispersal in 16 bryophyte taxa using a unique 35-year time series of environmental DNA (eDNA) data collected in Kiruna, northern Sweden. We used shotgun sequencing data from air filters and matched reads to all major organism groups, of which a high proportion were bryophyte reads.

We found consistent shifts in bryophyte phenology, such that most bryophyte taxa advanced their (i) start of season with 4 weeks on average, and (ii) mid-season with 6 weeks, ranging between 4 and 7 weeks. Changes at the season end were less consistent across the 16 bryophyte taxa, although seven of them showed phenological delays over time. Rising temperatures during the third and fourth quarters of the year preceding spore release were correlated with phenological shifts, suggesting that bryophytes may enter hibernation at later stages of sporophyte development, with warmer conditions promoting more advanced sporophyte maturation by the onset of spring. As a consequence of the phenological shifts, seasons during which spores were observed became several weeks longer over the studied time period for most taxa.

Synthesis: We conclude that the phenological shifts in our study suggest strong perturbations in bryophyte phenology, consistent with ongoing climate change. Our results demonstrate that studying airborne particles using eDNA methodology is a valuable complement to other monitoring methods, not the least in bryophytes and other less well-surveyed taxa.

Crop pests and diseases increasingly challenge the global food system. To prepare for and detect outbreaks, surveillance plays an important role. Traditional monitoring methods are often organism-specific, making large-scale monitoring of crop pathogens and pests impractical. We here investigate the potential for using shotgun sequencing of airborne eDNA for large-scale surveillance of crop pathogens and pests. We show that it is possible to detect DNA from all types of organisms in air, and that DNA can be classified down to species level. However, the accuracy of the identification is highly dependent on the quality of reference genomes of both the pathogens or pests, and their close relatives present in the region. Finally, we find that observed degree of crop damages correlate with amount of DNA from crop pathogens and pests in air, showing the promise of this approach for surveillance of all types of crop pathogens and pests.