skip to main content


Title: Microbial Dispersal, Including Bison Dung Vectored Dispersal, Increases Soil Microbial Diversity in a Grassland Ecosystem
Microbial communities display biogeographical patterns that are driven by local environmental conditions and dispersal limitation, but the relative importance of underlying dispersal mechanisms and their consequences on community structure are not well described. High dispersal rates can cause soil microbial communities to become more homogenous across space and therefore it is important to identify factors that promote dispersal. This study experimentally manipulated microbial dispersal within different land management treatments at a native tallgrass prairie site, by changing the relative openness of soil to dispersal and by simulating vector dispersal via bison dung addition. We deployed experimental soil bags with mesh open or closed to dispersal, and placed bison dung over a subset of these bags, to areas with three different land managements: active bison grazing and annual fire, annual fire but no bison grazing, and no bison grazing with infrequent fire. We expected microbial dispersal to be highest in grazed and burned environments, and that the addition of dung would consistently increase overall microbial richness and lead to homogenization of communities over time. Results show that dispersal rates, as the accumulation of taxa over the course of the 3-month experiment, increase taxonomic richness similarly in all land management treatments. Additionally, bison dung seems to be serving as a dispersal and homogenization vector, based on the consistently higher taxon richness and increased community similarity across contrasting grazing and fire treatments when dung is added. This finding also points to microbial dispersal as an important function that herbivores perform in grassland ecosystems, and in turn, as a function that was lost at a continental scale following bison extermination across the Great Plains of North America in the nineteenth century. This study is the first to detect that dispersal and vector dispersal by grazing mammals promote grassland soil microbial diversity and affect microbial community composition.  more » « less
Award ID(s):
1943492 2025849
NSF-PAR ID:
10330543
Author(s) / Creator(s):
;
Date Published:
Journal Name:
Frontiers in Microbiology
Volume:
13
ISSN:
1664-302X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    In the midst of an ongoing biodiversity crisis, much research has focused on species losses and their impacts on ecosystem functioning. The functional consequences (ecosystem response) of shifts in communities are shaped not only by changes in species richness, but also by compositional shifts that result from species losses and gains. Species differ in their contribution to ecosystem functioning, so species identity underlies the consequences of species losses and gains on ecosystem functions. Such research is critical to better predict the impact of disturbances on communities and ecosystems. We used the “Community Assembly and the Functioning of Ecosystems” (CAFE) approach, a modification of the Price equation to understand the functional consequences and relative effects of richness and composition changes in small nonvolant mammal and dung beetle communities as a result of two common disturbances in North American prairie restorations, prescribed fire and the reintroduction of large grazing mammals. Previous research in this system has shown dung beetles are critically important decomposers, while small mammals modulate much energy in prairie food webs. We found that dung beetle communities were more responsive to bison reintroduction and prescribed fires than small nonvolant mammals. Dung beetle richness increased after bison reintroduction, with higher dung beetle community biomass resulting from changes in remaining species (context‐dependent component) rather than species turnover (richness components); prescribed fire caused a minor increase in dung beetle biomass for the same reason. For small mammals, bison reintroduction reduced energy transfer through the loss of species, while prescribed fire had little impact on either small mammal richness or energy transfer. The CAFE approach demonstrates how bison reintroduction controls small nonvolant mammal communities by increasing prairie food web complexity, and increases dung beetle populations with possible benefits for soil health through dung mineralization and soil bioturbation. Prescribed fires, however, have little effect on small mammals and dung beetles, suggesting a resilience to fire. These findings illustrate the key role of re‐establishing historical disturbance regimes when restoring endangered prairie ecosystems and their ecological function.

     
    more » « less
  2. Abstract

    Knowledge of how habitat restoration shapes soil microbial communities often is limited despite their critical roles in ecosystem function. Soil community diversity and composition change after restoration, but the trajectory of these successional changes may be influenced by disturbances imposed for habitat management. We studied soil bacterial communities in a restored tallgrass prairie chronosequence for >6 years to document how diversity and composition changed with age, management through fire, and grazing by reintroduced bison, and in comparison to pre-restoration agricultural fields and remnant prairies. Soil C:N increased with restoration age and bison, and soil pH first increased and then declined with age, although bison weakened this pattern. Bacterial richness and diversity followed a similar hump-shaped pattern as soil pH, such that the oldest restorations approached the low diversity of remnant prairies. β-diversity patterns indicated that composition in older restorations with bison resembled bison-free sites, but over time they became more distinct. In contrast, younger restorations with bison maintained unique compositions throughout the study, suggesting bison disturbances may cause a different successional trajectory. We used a novel random forest approach to identify taxa that indicate these differences, finding that they were frequently associated with bacteria that respond to grazing in other grasslands.

     
    more » « less
  3. Summary

    Microbial communities will experience novel climates in the future. Dispersal is now recognized as a driver of microbial diversity and function, but our understanding of how dispersal influences responses to novel climates is limited. We experimentally tested how the exclusion of aerially dispersed fungi and bacteria altered the compositional and functional response of soil microbial communities to drought. We manipulated dispersal and drought by collecting aerially deposited microbes after precipitation events and subjecting soil mesocosms to either filter‐sterilized rain (no dispersal) or unfiltered rain (dispersal) and to either drought (25% ambient) or ambient rainfall for 6 months. We characterized community composition by sequencing 16S and ITS rRNA regions and function using community‐level physiological profiles. Treatments without dispersal had lower soil microbial biomass and metabolic diversity but higher bacterial and fungal species richness. Dispersal also altered soil community response to drought; drought had a stronger effect on bacterial (but not fungal) community composition, and induced greater functional loss, when dispersal was present. Surprisingly, neither immigrants nor drought‐tolerant taxa had higher abundance in dispersal treatments. We show experimentally that natural aerial dispersal rate alters soil microbial responses to disturbance. Changes in dispersal rates should be considered when predicting microbial responses to climate change.

     
    more » « less
  4. 1. Ecosystem restoration often focuses on re‐establishing species richness and diversity of native organisms. However, effective restoration requires re‐establishment of ecosystem functions and processes by all trophic levels. Functional trait descriptions of communities, including decomposer communities, may provide more comprehensive evaluations of restoration activities and management than taxonomic community metrics alone.

    2. We examined species and functional trait composition of dung beetle (Coleoptera: Scarabaeidae, Geotrupidae) communities across a 3–31 yearchronosequence of restored prairies, in which sites varied in the presence of re‐introduced bison and prescribed fire. We calculated functional diversity metrics and community‐weighted mean trait values using behavioural and morphological measurements. We also performed a dung decomposition experiment to measure an ecosystem function driven by these insects.

    3. Bison presence doubled beetle abundance and increased richness by 50%. Shannon diversity increased with restoration age, nearly doubling from the youngest to oldest restorations. Functional diversity was unchanged by site characteristics, except functional richness, which was reduced by bison and fire presence. Beetles were, on average, smaller in older restorations, although this pattern was weaker when bison were present.

    4. Dung decomposition was unaffected by site characteristics but increased with community weighted mean beetle mass. Dung decomposition was better predicted by mean trait values, suggesting that supporting large‐bodied species may be more important than species diversity in settings where maximizing decomposition function is a goal.

    5. Restoration managers should consider dung beetle communities and their functional characteristics when making management decisions, particularly where large grazers are a component of management strategies.

     
    more » « less
  5. Abstract

    Frequent fire and grazing by megafauna are important determinants of tallgrass prairie plant community structure. However, fire suppression and removal of native grazers have altered these natural disturbance regimes and changed grassland plant communities with potential long‐term consequences for soil carbon (C) and nitrogen (N) storage. We investigated multidecade changes in soil C and N pools in response to contrasting long‐term burning and grazing treatments. Fire suppression with or without grazers and exclusion of grazers in annually burned prairie increased soil C content and shifted the δ13C signature of soil C over time, concomitant with changes in plant community composition. Soil δ13C values indicated that increased soil C content was associated with an increased contribution from plants using a C3photosynthetic pathway (i.e., woody shrubs) under fire suppression. Soil N content also increased when fire was suppressed, relative to frequently burned grassland, but the rate of increase was slower when grazers were present. Additionally, changes in δ15N values suggested that grazing increased the openness of the N cycle, presumably due to greater N losses. By coupling long‐term fire and grazing treatments with plant community data and soil samples archived over three decades, we demonstrate that human‐caused changes to natural disturbance regimes in a tallgrass prairie significantly alter soil C and N cycles through belowground changes associated with shifts in the plant community. Since natural disturbance regimes have been altered in grasslands across the world, our results are relevant for understanding the long‐term biogeochemical consequences of these ongoing land use changes.

     
    more » « less