Biodiversity and ecosystem functioning in boreal streams:the effects of anthropogenic disturbances and naturally stressful environments

Abstract The effect of biodiversity loss and change on the functioning of ecosystems is one of the key questions in ecological research. For stream ecosystems, compelling evidence indicates that species diversity may enhance ecosystem functions. However, ecosystem functions are often regulated by the same environmental factors that also shape diversity; thus, a major challenge for ecologists is to separate the effects of biodiversity loss on the ecosystem functions from the direct effects of human induced disturbance. In this doctoral thesis, I studied how decomposer communities and ecosystem functions respond to human disturbances (nutrient enrichment, acidification) and a natural stressor (naturally low water pH). I also studied how human disturbances and natural stressors affect the phylogenetic structure of stream fungal communities. I showed that human disturbance had a strong impact on species dominance patterns by reducing species evenness. Species dominance patterns also explained the variation in decomposition rates. Changes in abiotic variables also had a direct effect on leaf decomposition rates. In the naturally acidic sites, human impact (land drainage) further decreased water pH and increased metal concentrations, thereby reducing leaf decomposition rates, whereas high nutrient concentrations enhanced leaf decomposition. Naturally low pH had no effect on decomposition rates. Decomposer community similarity was higher in drainage-impacted sites, but only in naturally acidic, not in circumneutral, streams. Human induced disturbance also modified the phylogenetic similarity of fungal decomposer communities, with communities in disturbed sites consisting of more closely related species when compared to those in circumneutral reference sites. Leaf litter decomposition showed greater temporal variation in human disturbed sites than in reference sites, whereas fungal community variability was similar in disturbed and reference sites. Thus, temporally replicated monitoring may be needed for a reliable assessment of human disturbance in streams. My thesis emphasizes that using both functional and taxonomic measures allows a more comprehensive assessment of biological responses to human disturbance.Tiivistelmä Biodiversiteetin väheneminen ja siitä seuraava ekosysteemin toiminnan heikkeneminen on eräs keskeisimmistä ekologisista kysymyksistä. Ekosysteemin toiminnot ovat kuitenkin monesti yhteydessä ympäristöolosuhteisiin, joten on vaikea erottaa vähentyneen biodiversiteetin ja ympäristöolojen suhteellista merkitystä ekosysteemien toimintoihin. Tässä väitöskirjatyössäni tutkin, kuinka virtavesien hajottajayhteisöt ja ekosysteemin toiminnot (lehtikarikkeen hajotus) muuttuvat valuma-alueen ihmistoimintojen myötä. Tutkin myös, kuinka luontainen stressi (matala pH) vaikuttaa yhteisöihin ja ekosysteemin toimintoihin. Tarkastelen myös akvaattisten sienten fylogeneettistä rakennetta ihmistoiminnan muuttamissa vesiympäristöissä. Osoitan tutkimuksissani, että ihmistoiminnoilla on vaikutuksia hajottajayhteisöiden kokonaisrunsauden jakautumiseen lajien kesken. Muutamien runsaiden lajien dominoimissa yhteisöissä lehtikarikkeen hajoaminen on tehokkaampaa kuin yhteisöissä, joissa lajien runsauserot ovat pienempiä. Myös ympäristöoloilla on vaikutus lehtikarikkeen hajotukseen. Luontaisesti happamissa puroissa metsäojituksen seurauksena lisääntynyt veden metallipitoisuus ja alhainen pH vähentävät hajotuksen määrää. Toisaalta joen korkea ravinnepitoisuus lisää hajotusta. Lehtikarikkeen hajotus vaihtelee enemmän vuosien välillä ihmistoimintojen muuttamissa virtavesissä kuin luonnontilaisissa vesissä. Toisaalta sieniyhteisöt pysyvät koostumukseltaan samankaltaisina vuosien välillä ihmistoiminnan muuttamissa paikoissa ja referenssipaikoissa. Tämä työ osoittaa, että toiminnallisten ja yhteisöihin perustuvien indikaattorien yhteiskäyttö antaa kokonaisvaltaisimman kuvan ihmistoimintojen vaikutuksesta virtavesien ekosysteemeihin

Data_Tolkkinen_etal

Rep set sequence data (fasta format), Environmental measurements data, and OTU table dat

Data from: Human disturbance increases functional but not structural variability of stream fungal communities

Temporal stability of ecosystem functions is often regulated by the same environmental factors that also shape diversity. Therefore, species diversity, ecosystem functions and their environmental regulators should be considered together to understand and predict the consequences of anthropogenic disturbances on ecosystems. We studied the influence of land-use disturbance (agriculture) and a natural stressor (low pH due to specific geology) on the temporal variability (variability among successive years) of fungal decomposer communities and leaf decomposition rates in streams. We used next-generation sequencing techniques (pyrosequencing) to determine the composition of fungal assemblages. Temporal variability of leaf decomposition was higher in human-disturbed streams than in circumneutral reference or naturally acidic sites, whereas the latter two did not differ. Fungal operational taxonomic unit (OTU) richness and evenness were lower in human-impacted sites than in circumneutral reference sites. However, there were no significant differences between stream types in the temporal variability of fungal community composition. Fungal OTU evenness was negatively and among-year variability of water chemistry positively related to temporal variability in leaf decomposition. Partial regressions showed that these two factors had independent effects on decomposition rates. Although the dominant OTUs in the disturbed streams were temporally stable, they did not maintain stable ecosystem functions, suggesting that variability in decomposition was driven mainly by changes in the metabolic responses of dominant taxa to environmental fluctuations. Our results show that leaf decomposition rates in reference sites vary little through time, supporting the use of leaf decomposition assays in bioassessment. Our results also highlight the importance of measuring not only the mean rates, but also temporal variability of process rates when assessing the influence of human disturbance on ecosystem functioning

Fungi originating from tree leaves contribute to fungal diversity of litter in streams

Abstract Biomass production and decomposition are key processes in ecology, where plants are primarily responsible for production and microbes act in decomposition. Trees harbor foliar microfungi living on and inside leaf tissues, epiphytes, and endophytes, respectively. Early researchers hypothesized that all fungal endophytes are parasites or latent saprophytes, which slowly colonize the leaf tissues for decomposition. While this has been proven for some strains in the terrestrial environment, it is not known whether foliar microfungi from terrestrial origin can survive or perform decomposition in the aquatic environment. On the other hand, aquatic hyphomycetes, fungi which decompose organic material in stream environments, have been suggested to have a plant-associated life phase. Our aim was to study how much the fungal communities of leaves and litter submerged in streams overlap. Ergosterol content on litter, which is an estimator of fungal biomass, was 5–14 times higher in submerged litter than in senescent leaves, indicating active fungal colonization. Leaves generally harbored a different microbiome prior to than after submergence in streams. The Chao1 richness was significantly higher (93.7 vs. 60.7, p = 0.004) and there were more observed operational taxonomic units (OTUs) (78.3 vs. 47.4, p = 0.004) in senescent leaves than in stream-immersed litter. There were more Leotiomycetes (9%, p = 0.014) in the litter. We identified a group of 35 fungi (65%) with both plant- and water-associated lifestyles. Of these, eight taxa had no previous references to water, such as lichenicolous fungi. Six OTUs were classified within Glomeromycota, known as obligate root symbionts with no previous records from leaves. Five members of Basidiomycota, which are rare in aquatic environments, were identified in the stream-immersed litter only. Overall, our study demonstrates that foliar microfungi contribute to fungal diversity in submerged litter