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Title: Precipitation, Not Land Use, Primarily Determines the Composition of Both Plant and Phyllosphere Fungal Communities

Plant communities and fungi inhabiting their phyllospheres change along precipitation gradients and often respond to changes in land use. Many studies have focused on the changes in foliar fungal communities on specific plant species, however, few have addressed the association between whole plant communities and their phyllosphere fungi. We sampled plant communities and associated phyllosphere fungal communities in native prairie remnants and post-agricultural sites across the steep precipitation gradient in the central plains in Kansas, USA. Plant community cover data and MiSeq ITS2 metabarcode data of the phyllosphere fungal communities indicated that both plant and fungal community composition respond strongly to mean annual precipitation (MAP), but less so to land use (native prairie remnants vs. post-agricultural sites). However, plant and fungal diversity were greater in the native remnant prairies than in post-agricultural sites. Overall, both plant and fungal diversity increased with MAP and the communities in the arid and mesic parts of the gradient were distinct. Analyses of the linkages between plant and fungal communities (Mantel and Procrustes tests) identified strong correlations between the composition of the two. However, despite the strong correlations, regression models with plant richness, diversity, or composition (ordination axis scores) and land use as explanatory variables for fungal diversity and evenness did not improve the models compared to those with precipitation and land use (ΔAIC < 2), even though the explanatory power of some plant variables was greater than that of MAP as measured by R2. Indicator taxon analyses suggest that grass species are the primary taxa that differ in the plant communities. Similar analyses of the phyllosphere fungi indicated that many plant pathogens are disproportionately abundant either in the arid or mesic environments. Although decoupling the drivers of fungal communities and their composition – whether abiotic or host-dependent – remains a challenge, our study highlights the distinct community responses to precipitation and the tight tracking of the plant communities by their associated fungal symbionts.

 
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Award ID(s):
2025849 1656006
NSF-PAR ID:
10473337
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
Frontiers
Date Published:
Journal Name:
Frontiers in Fungal Biology
Volume:
3
ISSN:
2673-6128
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Abstract

    The consequences of land‐use change for savanna biodiversity remain undocumented in most regions of tropical Asia. One such region is western Maharashtra, India, where old‐growth savannas occupy a broad rainfall gradient and are increasingly rare due to agricultural conversion and afforestation.

    To understand the consequences of land‐use change, we sampled herbaceous plant communities of old‐growth savannas and three alternative land‐use types: tree plantations, tillage agriculture and agricultural fallows (n = 15 sites per type). Study sites spanned 457 to 1954 mm of mean annual precipitation—corresponding to the typical rainfall range of mesic savannas globally.

    Across the rainfall gradient, we found consistent declines in old‐growth savanna plant communities due to land‐use change. Local‐scale native species richness dropped from a mean of 12 species/m2in old‐growth savannas to 8, 6 and 3 species/m2in tree plantations, fallows and tillage agriculture, respectively. Cover of native plants declined from a mean of 49% in old‐growth savannas to 27% in both tree plantations and fallows, and 4% in tillage agriculture. Reduced native cover coincided with increased cover of invasive species in tree plantations (18%), fallows (18%) and tillage agriculture (3%).

    In analyses of community composition, tillage agriculture was most dissimilar to old‐growth savannas, while tree plantations and fallows showed intermediate dissimilarity. These compositional changes were driven partly by the loss of characteristic savanna species: 65 species recorded in old‐growth savannas were absent in other land uses. Indicator analysis revealed 21 old‐growth species, comprised mostly of native savanna specialists. Indicators of tree plantations (nine species) and fallows (13 species) were both invasive and native species, while the two indicators of tillage agriculture were invasive. As reflective of declines in savanna communities, mean native perennial graminoid cover of 27% in old‐growth savannas dropped to 9%, 7%, and 0.1% in tree plantations, fallows and tillage agriculture, respectively.

    Synthesis. Agricultural conversion and afforestation of old‐growth savannas in India destroys and degrades herbaceous plant communities that do not spontaneously recover on fallowed land. Efforts to conserve India's native biodiversity should encompass the country's widespread savanna biome and seek to limit conversion of irreplaceable old‐growth savannas.

     
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We also used the Tukey–Kramer method to compare the frequency distributions of TDP concentrations in all of the soil leachate samples with concentrations in lakes, streams, and groundwater wells, since each sample category had very different numbers of measurements. Individual spreadsheets in “data table_leaching_dissolved organic carbon and nitrogen.xls” 1.    annual precip_drainage 2.    biomass_corn, perennial grasses 3.    biomass_poplar 4.    annual N leaching _vol-wtd conc 5.    Summary_N leached 6.    annual DOC leachin_vol-wtd conc 7.    growing season length 8.    correlation_nh4 VS no3 9.    correlations_don VS no3_doc VS don Each spreadsheet is described below along with an explanation of variates. Note that ‘nan’ indicate data are missing or not available. First row indicates header; second row indicates units 1. Spreadsheet: annual precip_drainage Description: Precipitation measured from nearby Kellogg Biological Station (KBS) Long Term Ecological Research (LTER) Weather station, over 2009-2016 study period. Data shown in Figure 1; original data source for precipitation (https://lter.kbs.msu.edu/datatables/7). Drainage estimated from SALUS crop model. Note that drainage is percolation out of the root zone (0-125 cm). Annual precipitation and drainage values shown here are calculated for growing and non-growing crop periods. Variate    Description year    year of the observation crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” precip_G    precipitation during growing period (milliMeter) precip_NG    precipitation during non-growing period (milliMeter) drainage_G    drainage during growing period (milliMeter) drainage_NG    drainage during non-growing period (milliMeter)      2. Spreadsheet: biomass_corn, perennial grasses Description: Maximum aboveground biomass measurements from corn, switchgrass, miscanthus, native grass and restored prairie plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2009-2015. Data shown in Figure 2.   Variate    Description year    year of the observation date    day of the observation (mm/dd/yyyy) crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” replicate    each crop has four replicated plots, R1, R2, R3 and R4 station    stations (S1, S2 and S3) of samplings within the plot. For more details, refer to link (https://data.sustainability.glbrc.org/protocols/156) species    plant species that are rooted within the quadrat during the time of maximum biomass harvest. See protocol for more information, refer to link (http://lter.kbs.msu.edu/datatables/36) For maize biomass, grain and whole biomass reported in the paper (weed biomass or surface litter are excluded). Surface litter biomass not included in any crops; weed biomass not included in switchgrass and miscanthus, but included in grass mixture and prairie. fraction    Fraction of biomass biomass_plot    biomass per plot on dry-weight basis (Grams_Per_SquareMeter) biomass_ha    biomass (megaGrams_Per_Hectare) by multiplying column biomass per plot with 0.01 3. Spreadsheet: biomass_poplar Description: Maximum aboveground biomass measurements from poplar plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2009-2015. Data shown in Figure 2. Note that poplar biomass was estimated from crop growth curves until the poplar was harvested in the winter of 2013-14. Variate    Description year    year of the observation method    methods of poplar biomass sampling date    day of the observation (mm/dd/yyyy) replicate    each crop has four replicated plots, R1, R2, R3 and R4 diameter_at_ground    poplar diameter (milliMeter) at the ground diameter_at_15cm    poplar diameter (milliMeter) at 15 cm height biomass_tree    biomass per plot (Grams_Per_Tree) biomass_ha    biomass (megaGrams_Per_Hectare) by multiplying biomass per tree with 0.01 4. Spreadsheet: annual N leaching_vol-wtd conc Description: Annual leaching rate (kiloGrams_N_Per_Hectare) and volume-weighted mean N concentrations (milliGrams_N_Per_Liter) of nitrate (no3) and dissolved organic nitrogen (don) in the leachate samples collected from corn, switchgrass, miscanthus, native grass, restored prairie and poplar plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2009-2016. Data for nitrogen leached and volume-wtd mean N concentration shown in Figure 3a and Figure 3b, respectively. Note that ammonium (nh4) concentration were much lower and often undetectable (<0.07 milliGrams_N_Per_Liter). Also note that in 2009 and 2010 crop-years, data from some replicates are missing.    Variate    Description crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” crop-year    year of the observation replicate    each crop has four replicated plots, R1, R2, R3 and R4 no3 leached    annual leaching rates of nitrate (kiloGrams_N_Per_Hectare) don leached    annual leaching rates of don (kiloGrams_N_Per_Hectare) vol-wtd no3 conc.    Volume-weighted mean no3 concentration (milliGrams_N_Per_Liter) vol-wtd don conc.    Volume-weighted mean don concentration (milliGrams_N_Per_Liter) 5. Spreadsheet: summary_N leached Description: Summary of total amount and forms of N leached (kiloGrams_N_Per_Hectare) and the percent of applied N lost to leaching over the seven years for corn, switchgrass, miscanthus, native grass, restored prairie and poplar plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2009-2016. Data for nitrogen amount leached shown in Figure 4a and percent of applied N lost shown in Figure 4b. Note the fraction of unleached N includes in harvest, accumulation in root biomass, soil organic matter or gaseous N emissions were not measured in the study. Variate    Description crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” no3 leached    annual leaching rates of nitrate (kiloGrams_N_Per_Hectare) don leached    annual leaching rates of don (kiloGrams_N_Per_Hectare) N unleached    N unleached (kiloGrams_N_Per_Hectare) in other sources are not studied % of N applied N lost to leaching    % of N applied N lost to leaching 6. Spreadsheet: annual DOC leachin_vol-wtd conc Description: Annual leaching rate (kiloGrams_Per_Hectare) and volume-weighted mean N concentrations (milliGrams_Per_Liter) of dissolved organic carbon (DOC) in the leachate samples collected from corn, switchgrass, miscanthus, native grass, restored prairie and poplar plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2009-2016. Data for DOC leached and volume-wtd mean DOC concentration shown in Figure 5a and Figure 5b, respectively. Note that in 2009 and 2010 crop-years, water samples were not available for DOC measurements.     Variate    Description crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” crop-year    year of the observation replicate    each crop has four replicated plots, R1, R2, R3 and R4 doc leached    annual leaching rates of nitrate (kiloGrams_Per_Hectare) vol-wtd doc conc.    volume-weighted mean doc concentration (milliGrams_Per_Liter) 7. Spreadsheet: growing season length Description: Growing season length (days) of corn, switchgrass, miscanthus, native grass, restored prairie and poplar plots in the Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2009-2015. Date shown in Figure S2. Note that growing season is from the date of planting or emergence to the date of harvest (or leaf senescence in case of poplar).   Variate    Description crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” year    year of the observation growing season length    growing season length (days) 8. Spreadsheet: correlation_nh4 VS no3 Description: Correlation of ammonium (nh4+) and nitrate (no3-) concentrations (milliGrams_N_Per_Liter) in the leachate samples from corn, switchgrass, miscanthus, native grass, restored prairie and poplar plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2013-2015. Data shown in Figure S3. Note that nh4+ concentration in the leachates was very low compared to no3- and don concentration and often undetectable in three crop-years (2013-2015) when measurements are available. Variate    Description crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” date    date of the observation (mm/dd/yyyy) replicate    each crop has four replicated plots, R1, R2, R3 and R4 nh4 conc    nh4 concentration (milliGrams_N_Per_Liter) no3 conc    no3 concentration (milliGrams_N_Per_Liter)   9. Spreadsheet: correlations_don VS no3_doc VS don Description: Correlations of don and nitrate concentrations (milliGrams_N_Per_Liter); and doc (milliGrams_Per_Liter) and don concentrations (milliGrams_N_Per_Liter) in the leachate samples of corn, switchgrass, miscanthus, native grass, restored prairie and poplar plots in Great Lakes Bioenergy Research Center (GLBRC) Biomass Cropping System Experiment (BCSE) during 2013-2015. Data of correlation of don and nitrate concentrations shown in Figure S4 a and doc and don concentrations shown in Figure S4 b. 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  5. Abstract

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