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Title: Defoliation severity is positively related to soil solution nitrogen availability and negatively related to soil nitrogen concentrations following a multi-year invasive insect irruption
Abstract Understanding connections between ecosystem nitrogen (N) cycling and invasive insect defoliation could facilitate the prediction of disturbance impacts across a range of spatial scales. In this study we investigated relationships between ecosystem N cycling and tree defoliation during a recent 2015–18 irruption of invasive gypsy moth caterpillars (Lymantria dispar), which can cause tree stress and sometimes mortality following multiple years of defoliation. Nitrogen is a critical nutrient that limits the growth of caterpillars and plants in temperate forests. In this study, we assessed the associations among N concentrations, soil solution N availability and defoliation intensity by L. dispar at the scale of individual trees and forest plots. We measured leaf and soil N concentrations and soil solution inorganic N availability among individual red oak trees (Quercus rubra) in Amherst, MA and across a network of forest plots in Central Massachusetts. We combined these field data with estimated defoliation severity derived from Landsat imagery to assess relationships between plot-scale defoliation and ecosystem N cycling. We found that trees in soil with lower N concentrations experienced more herbivory than trees in soil with higher N concentrations. Additionally, forest plots with lower N soil were correlated with more severe L. dispar defoliation, which matched the tree-level relationship. The amount of inorganic N in soil solution was strongly positively correlated with defoliation intensity and the number of sequential years of defoliation. These results suggested that higher ecosystem N pools might promote the resistance of oak trees to L. dispar defoliation and that defoliation severity across multiple years is associated with a linear increase in soil solution inorganic N.  more » « less
Award ID(s):
1832210 1950364
NSF-PAR ID:
10211404
Author(s) / Creator(s):
; ; ; ; ;
Editor(s):
Atkins, Jeff
Date Published:
Journal Name:
AoB PLANTS
Volume:
12
Issue:
6
ISSN:
2041-2851
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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    Carbon starvation posits that defoliation‐ and drought‐induced mortality results from drawing down stored non‐structural carbohydrates (NSCs), but evidence is mixed, and few studies evaluate mortality directly. We tested the relationships among defoliation severity, NSC drawdown and tree mortality by measuring NSCs in mature oak trees defoliated by an invasive insect,Lymantria dispar, across a natural gradient of defoliation severity.

    We collected stem and root samples from mature oaks (Quercus rubraandQ.alba) in interior forests (n = 34) and forest edges (n = 47) in central Massachusetts, USA. Total NSC (TNC; sugar + starch) stores were analysed with respect to tree size, species and defoliation severity, which ranged between 5% and 100%.

    TNC stores declined significantly with increasingly severe defoliation. Forest edge trees had higher TNC stores that were less sensitive to defoliation than interior forest trees, although this may be a result of differing defoliation history. Furthermore, we observed a mortality threshold of 1.5% dry weight TNC.

    Our study draws a direct link between insect defoliation and TNC reserves and defines a TNC threshold below which mortality is highly likely. These findings advance understanding and improve model parametrization of tree response to insect outbreaks, an increasing threat with globalization and climate change.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
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Soil water TDP concentrations were usually below levels where eutrophication of surface waters is frequently observed (> 0.02 mg L−1) but often higher than in deep groundwater or nearby streams and lakes. Rates of P leaching, estimated from measured concentrations and modeled drainage, did not differ statistically among cropping systems across years; 7-year cropping system means ranged from 0.035 to 0.072 kg P ha−1 year−1 with large interannual variation. Leached P was positively related to STP, which decreased over the 7 years in all systems. These results indicate that both P-fertilized and unfertilized cropping systems may leach legacy P from past cropland management. Experimental details The Biofuel Cropping System Experiment (BCSE) is located at the W.K. Kellogg Biological Station (KBS) (42.3956° N, 85.3749° W; elevation 288 m asl) in southwestern Michigan, USA. 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Volume-weighted mean TDP concentrations in leachate for each crop-year and for the entire 7-year study period were calculated as the total dissolved P leaching flux (kg ha−1) divided by the total drainage (m3 ha−1). One-way ANOVA with time (crop-year) as the fixed factor was conducted to compare total annual drainage rates, P leaching rates, volume-weighted mean TDP concentrations, and maximum aboveground biomass among the cropping systems over all seven crop-years as well as with TDP concentrations from local lakes, streams, and groundwater wells. When a significant (α = 0.05) difference was detected among the groups, we used the Tukey honest significant difference (HSD) post-hoc test to make pairwise comparisons among the groups. In the case of maximum aboveground biomass, we used the Tukey–Kramer method to make pairwise comparisons among the groups because the absence of poplar data after the 2013 harvest resulted in unequal sample sizes. 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. Variate    Description crop    “corn” “switchgrass” “miscanthus” “nativegrass” “restored prairie” “poplar” year    year of the observation don    don concentration (milliGrams_N_Per_Liter) no3     no3 concentration (milliGrams_N_Per_Liter) doc    doc concentration (milliGrams_Per_Liter) 
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  4. The Baltimore Ecosystem Study (BES) has established a network of long-term permanent biogeochemical study plots. These plots will provide long-term data on vegetation, soil and hydrologic processes in the key ecosystem types within the urban ecosystem. The current network of study plots includes eight forest plots, chosen to represent the range of forest conditions in the area, and four grass plots. These plots are complemented by a network of 200 less intensive study plots located across the Baltimore metropolitan area. Plots are currently instrumented with lysimeters (drainage and tension) to sample soil solution chemistry, time domain reflectometry probes to measure soil moisture, dataloggers to measure and record soil temperature and trace gas flux chambers to measure the flux of carbon dioxide, nitrous oxide and methane from soil to the atmosphere. Measurements of in situ nitrogen mineralization, nitrification and denitrification were made at approximately monthly intervals from Fall 1998 - Fall 2000. Detailed vegetation characterization (all layers) was done in summer 1998. Data from these plots has been published in Groffman et al. (2006, 2009) and Groffman and Pouyat (2009). In November of 1998 four rural, forested plots were established at Oregon Ridge Park in Baltimore County northeast of the Gwynns Falls Watershed. Oregon Ridge Park contains Pond Branch, the forested reference watershed for BES. Two of these four plots are located on the top of a slope; the other two are located midway up the slope. In June of 2010 measurements at the mid-slope sites on Pond Branch were discontinued. Monuments and equipment remain at the two plots. These plots were replaced with two lowland riparian plots; Oregon upper riparian and Oregon lower riparian. Each riparian sites has four 5 cm by 1-2.5 meter depth slotted wells laid perpendicular to the stream, four tension lysimeters at 10 cm depth, five time domain reflectometry probes, and four trace gas flux chambers in the two dominant microtopographic features of the riparian zones - high spots (hummocks) and low spots (hollows). Four urban, forested plots were established in November 1998, two at Leakin Park and two adjacent to Hillsdale Park in west Baltimore City in the Gwynns Falls. One of the plots in Hillsdale Park was abandoned in 2004 due to continued vandalism. In May 1999 two grass, lawn plots were established at McDonogh School in Baltimore County west of the city in the Gwynns Falls. One of these plots is an extremely low intensity management area (mowed once or twice a year) and one is in a low intensity management area (frequent mowing, no fertilizer or herbicide use). In 2009, the McDonogh plots were abandoned due to management changes at the school. Two grass lawn plots were established on the campus of the University of Maryland, Baltimore County (UMBC) in fall 2000. One of these plots is in a medium intensity management area (frequent mowing, moderate applications of fertilizer and herbicides) and one is in a high intensity management area (frequent mowing, high applications of fertilizer and herbicides). Literature Cited Bowden R, Steudler P, Melillo J and Aber J. 1990. Annual nitrous oxide fluxes from temperate forest soils in the northeastern United States. J. Geophys. Res.-Atmos. 95, 13997 14005. Driscoll CT, Fuller RD and Simone DM (1988) Longitudinal variations in trace metal concentrations in a northern forested ecosystem. J. Environ. Qual. 17: 101-107 Goldman, M. B., P. M. Groffman, R. V. Pouyat, M. J. McDonnell, and S. T. A. Pickett. 1995. CH4 uptake and N availability in forest soils along an urban to rural gradient. Soil Biology and Biochemistry 27:281-286. Groffman PM, Holland E, Myrold DD, Robertson GP and Zou X (1999) Denitrification. In: Robertson GP, Bledsoe CS, Coleman DC and Sollins P (Eds) Standard Soil Methods for Long Term Ecological Research. (pp 272-290). Oxford University Press, New York Groffman PM, Pouyat RV, Cadenasso ML, Zipperer WC, Szlavecz K, Yesilonis IC,. Band LE and Brush GS. 2006. Land use context and natural soil controls on plant community composition and soil nitrogen and carbon dynamics in urban and rural forests. Forest Ecology and Management 236:177-192. Groffman, P.M., C.O. Williams, R.V. Pouyat, L.E. Band and I.C. Yesilonis. 2009. Nitrate leaching and nitrous oxide flux in urban forests and grasslands. Journal of Environmental Quality 38:1848-1860. Groffman, P.M. and R.V. Pouyat. 2009. Methane uptake in urban forests and lawns. Environmental Science and Technology 43:5229-5235. DOI: 10.1021/es803720h. Holland EA, Boone R, Greenberg J, Groffman PM and Robertson GP (1999) Measurement of Soil CO2, N2O and CH4 exchange. In: Robertson GP, Bledsoe CS, Coleman DC and Sollins P (Eds) Standard Soil Methods for Long Term Ecological Research. (pp 258-271). Oxford University Press, New York Robertson GP, Wedin D, Groffman PM, Blair JM, Holland EA, Nadelhoffer KJ and. Harris D. 1999. Soil carbon and nitrogen availability: Nitrogen mineralization, nitrification and carbon turnover. In: Standard Soil Methods for Long Term Ecological Research (Robertson GP, Bledsoe CS, Coleman DC and Sollins P (Eds) Standard Soil Methods for Long Term Ecological Research. (pp 258-271). Oxford University Press, New York Savva, Y., K. Szlavecz, R. V. Pouyat, P. M. Groffman, and G. Heisler. 2010. Effects of land use and vegetation cover on soil temperature in an urban ecosystem. Soil Science Society of America Journal 74:469-480." 
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  5. Abstract

    Plant–fungal associations strongly influence forest carbon and nitrogen cycling. The prevailing framework for understanding these relationships is through the relative abundance of arbuscular (AM) versus ectomycorrhizal (EcM) trees. Ericoid mycorrhizal (ErM) shrubs are also common in forests and interactions between co‐occurring ErM shrubs and AM and EcM trees could shift soil biogeochemical responses. Here we test hypotheses that the effects of ErM shrubs on soil carbon and nitrogen either extend or are redundant with those of EcM trees.

    Using regional vegetation inventory data (>3,500 plot observations) we evaluated the frequency, richness and relative abundance of ErM plants in temperate forests in the eastern United States and examined their relationship with EcM plant cover. We then used surface soil (7 cm) data from 414 plots within a single forest to analyse relationships between ErM plant cover, relative EcM tree basal area and soil carbon and nitrogen concentrations while accounting for other biogeochemical controls, such as soil moisture.

    At both scales, we found a positive relationship between ErM and EcM plants, and the majority of ErM plants were in the shrub layer. Within the forest site, ErM plants strongly modulated tree mycorrhizal dominance effects. We found negative relationships between EcM relative basal area and soil carbon and nitrogen concentrations, but these relationships were weak to negligible in the absence of ErM plants. Both EcM relative basal area and ErM plant cover were positively associated with the soil carbon‐to‐nitrogen ratio. However, this relationship was driven by relatively lower nitrogen for EcM trees and higher carbon for ErM plants. As such, the functional effects of ErM plants on soil biogeochemistry neither extended nor were redundant with those of EcM trees.

    Synthesis. We found that ErM shrubs strongly influenced the relationship between tree mycorrhizal associations and soil biogeochemistry, and the effects of ErM shrubs and EcM trees on carbon and nitrogen were functionally distinct. Our findings suggest that ErM shrubs could confound interpretation of AM versus EcM tree effects in ecosystems where they co‐occur but also bolster growing calls to consider mycorrhizal functional types as variables that strongly influence forest biogeochemistry.

     
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